In vitro Characteristics of Heterogeneous Equine Hoof Progenitor Cell Isolates.
Abstract: Damage to an ectodermal-mesodermal interface like that in the equine hoof and human finger nail bed can permanently alter tissue structure and associated function. The purpose of this study was to establish and validate culture of primary progenitor cell isolates from the ectodermal-mesodermal tissue junction in equine hooves, the stratum internum, with and without chronic inflammation known to contribute to lifelong tissue defects. The following were evaluated in hoof stratum internum cell isolates up to 5 cell passages (P): expansion capacity by cell doublings and doubling time; plasticity with multi-lineage differentiation and colony-forming unit (CFU) frequency percentage; immunophenotype with immunocytochemistry and flow cytometry; gene expression with RT-PCR; and ultrastructure with transmission electron microscopy. The presence of keratin (K)14, 15 and K19 as well as cluster of differentiation (CD)44 and CD29 was determined with immunohistochemistry. To confirm extracellular matrix (ECM) formation, cell-scaffold (polyethylene glycol/poly-L-lactic acid and tricalcium phosphate/hydroxyapatite) constructs were evaluated with scanning electron microscopy 9 weeks after implantation in athymic mice. Cultured cells had characteristic progenitor cell morphology, expansion, CFU frequency percentage and adipocytic, osteoblastic, and neurocytic differentiation capacity. CD44, CD29, K14, K15 and K19 proteins were present in native hoof stratum internum. Cultured cells also expressed K15, K19 and desmogleins 1 and 3. Gene expression of CD105, CD44, K14, K15, sex determining region Y-box 2 (SOX2) and octamer-binding transcription factor 4 (OCT4) was confirmed . Cultured cells had large, eccentric nuclei, elongated mitochondria, and intracellular vacuoles. Scaffold implants with cells contained fibrous ECM 9 weeks after implantation compared to little or none on acellular scaffolds. expansion and plasticity and ECM deposition of heterogeneous, immature cell isolates from the ectodermal-mesodermal tissue interface of normal and chronically inflamed hooves are typical of primary cell isolates from other adult tissues, and they appear to have both mesodermal and ectodermal qualities . These results establish a unique cell culture model to target preventative and restorative therapies for ectodermal-mesodermal tissue junctions.
Publication Date: 2019-07-11 PubMed ID: 31355191PubMed Central: PMC6637248DOI: 10.3389/fbioe.2019.00155Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Animal Studies
- Cell Culture
- Cells
- Equine Health
- Extracellular matrix
- Flow Cytometry
- Gene Expression
- Immunocytochemistry
- Immunohistochemistry
- In Vitro Research
- Inflammation
- Mesenchymal Cells
- Microscopy
- Real-Time PCR
- Scanning Electron Microscopy
- Stem Cells
- Tissue
- Transmission Electron Microscopy
- Veterinary Medicine
- Veterinary Research
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article presents a study that focuses on the in vitro characteristics and cultivation of primary progenitor cell groups sourced from the stratum internum in equine hooves, a layer similar to human fingernails. The study explored these traits both in the context of normal tissues and in tissues suffering from chronic inflammation, in order to comprehend their potential for restorative therapies for tissues that are ectodermal-mesodermal in nature.
Research Methodology
- The investigators evaluated the properties of hoof stratum internum cell isolates for up to five passages in terms of expansion rate, differentiation capacity, CFU frequency, immunotype, gene expression, and ultrastructure.
- A combination of immunocytochemistry, flow cytometry, RT-PCR, and transmission electron microscopy was used for these experiments.
- The presence of various keratin subtypes (K14, K15, K19) and cluster of differentiation (CD) markers (CD29 and CD44) was determined using immunohistochemistry.
- To ascertain the formation of the extracellular matrix (ECM), cell-scaffold constructs were placed into athymic mice and subjected to scanning electron microscopy nine weeks post-implantation.
Research Findings
- The results revealed that the cultured cells had typical progenitor cell morphology, expansion capacity, CFU percentage, and the capability to differentiate into adipocytic, osteoblastic, and neurocytic lineages.
- In the native hoof stratum internum, CD44, CD29, K14, K15, and K19 proteins were detected. Additionally, the cultured cells demonstrated K15, K19, and desmogleins 1 and 3.
- Gene expression of CD105, CD44, K14, K15, SOX2, and OCT4 was authenticated.
- Cellular analysis showed large, eccentric nuclei, elongated mitochondria, and intracellular vacuoles in the cultured cells.
- The implanted scaffolds containing cells displayed fibrous ECM nine weeks after implantation, contrasting with acellular scaffolds, which exhibited little to no ECM.
Conclusions and Implications
- The study confirms the capacity for expansion, differentiation, and ECM formation among heterogeneous, immature cell isolates sourced from the ectodermal-mesodermal tissue of both normal and chronically inflamed equine hooves.
- This suggests these characteristics closely match those of primary cell isolates from other adult tissues, demonstrating a combination of mesodermal and ectodermal qualities.
- These findings pave the way for the development of a unique cell culture model, which could be instrumental in creating preventative and restorative therapies for ectodermal-mesodermal tissue junctions.
Cite This Article
APA
Yang Q, Pinto VMR, Duan W, Paxton EE, Dessauer JH, Ryan W, Lopez MJ.
(2019).
In vitro Characteristics of Heterogeneous Equine Hoof Progenitor Cell Isolates.
Front Bioeng Biotechnol, 7, 155.
https://doi.org/10.3389/fbioe.2019.00155 Publication
Researcher Affiliations
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
- Laboratory for Equine and Comparative Orthopedic Research, Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, United States.
References
This article includes 116 references
- Abbas O, Richards JE, Yaar R, Mahalingam M. Stem cell markers (cytokeratin 15, cytokeratin 19 and p63) in in situ and invasive cutaneous epithelial lesions.. Mod Pathol 2011 Jan;24(1):90-7.
- Alipour F, Parham A, Kazemi Mehrjerdi H, Dehghani H. Equine adipose-derived mesenchymal stem cells: phenotype and growth characteristics, gene expression profile and differentiation potentials.. Cell J 2015 Winter;16(4):456-65.
- Altschuler SJ, Wu LF. Cellular heterogeneity: do differences make a difference?. Cell 2010 May 14;141(4):559-63.
- Amagai M, Stanley JR. Desmoglein as a target in skin disease and beyond.. J Invest Dermatol 2012 Mar;132(3 Pt 2):776-84.
- Amini S, Fathi F, Mobalegi J, Sofimajidpour H, Ghadimi T. The expressions of stem cell markers: Oct4, Nanog, Sox2, nucleostemin, Bmi, Zfx, Tcl1, Tbx3, Dppa4, and Esrrb in bladder, colon, and prostate cancer, and certain cancer cell lines.. Anat Cell Biol 2014 Mar;47(1):1-11.
- Anderson TM, McIlwraith CW. Longitudinal development of equine conformation from weanling to age 3 years in the Thoroughbred.. Equine Vet J 2004 Nov;36(7):563-70.
- Arsenian S, Weinhold B, Oelgeschläger M, Rüther U, Nordheim A. Serum response factor is essential for mesoderm formation during mouse embryogenesis.. EMBO J 1998 Nov 2;17(21):6289-99.
- Atala A, Irvine DJ, Moses M, Shaunak S. Wound Healing Versus Regeneration: Role of the Tissue Environment in Regenerative Medicine.. MRS Bull 2010 Aug 1;35(8).
- Bailey SR. Acute equine laminitis: Exciting prospects afoot.. Vet J 2015 Nov;206(2):121-2.
- Barreto-Vianna A. R., Oliveira L. S., Leonardo A. S., Santana M. I., Godoy R. F., De Lima E. M.. Density of primary and secondary epidermal laminae of equine hoof. Pesqui. Vet. Bras. 33, 543–548.
- Bharathi RR, Bajantri B. Nail bed injuries and deformities of nail.. Indian J Plast Surg 2011 May;44(2):197-202.
- Bose A, Teh MT, Mackenzie IC, Waseem A. Keratin k15 as a biomarker of epidermal stem cells.. Int J Mol Sci 2013 Sep 25;14(10):19385-98.
- Bourguignon LY, Wong G, Earle C, Chen L. Hyaluronan-CD44v3 interaction with Oct4-Sox2-Nanog promotes miR-302 expression leading to self-renewal, clonal formation, and cisplatin resistance in cancer stem cells from head and neck squamous cell carcinoma.. J Biol Chem 2012 Sep 21;287(39):32800-24.
- Bourzac C, Smith LC, Vincent P, Beauchamp G, Lavoie JP, Laverty S. Isolation of equine bone marrow-derived mesenchymal stem cells: a comparison between three protocols.. Equine Vet J 2010 Sep;42(6):519-27.
- Bragulla HH, Homberger DG. Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia.. J Anat 2009 Apr;214(4):516-59.
- Broeckx SY, Maes S, Martinello T, Aerts D, Chiers K, Mariën T, Patruno M, Franco-Obregón A, Spaas JH. Equine epidermis: a source of epithelial-like stem/progenitor cells with in vitro and in vivo regenerative capacities.. Stem Cells Dev 2014 May 15;23(10):1134-48.
- Campello S, Scorrano L. Mitochondrial shape changes: orchestrating cell pathophysiology.. EMBO Rep 2010 Sep;11(9):678-84.
- Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine.. J Cell Physiol 2007 Nov;213(2):341-7.
- Colter DC, Sekiya I, Prockop DJ. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells.. Proc Natl Acad Sci U S A 2001 Jul 3;98(14):7841-5.
- Corradetti B, Lange-Consiglio A, Barucca M, Cremonesi F, Bizzaro D. Size-sieved subpopulations of mesenchymal stem cells from intervascular and perivascular equine umbilical cord matrix.. Cell Prolif 2011 Aug;44(4):330-42.
- Daradka M, Pollitt CC. Epidermal cell proliferation in the equine hoof wall.. Equine Vet J 2004 Apr;36(3):236-41.
- de Mattos Carvalho A, Alves AL, Golim MA, Moroz A, Hussni CA, de Oliveira PG, Deffune E. Isolation and immunophenotypic characterization of mesenchymal stem cells derived from equine species adipose tissue.. Vet Immunol Immunopathol 2009 Dec 15;132(2-4):303-6.
- Ding G, Liu Y, Wang W, Wei F, Liu D, Fan Z, An Y, Zhang C, Wang S. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine.. Stem Cells 2010 Oct;28(10):1829-38.
- Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.. Cytotherapy 2006;8(4):315-7.
- Duan W, Chen C, Haque M, Hayes D, Lopez MJ. Polymer-mineral scaffold augments in vivo equine multipotent stromal cell osteogenesis.. Stem Cell Res Ther 2018 Mar 9;9(1):60.
- Duan W, Lopez MJ. Effects of Cryopreservation on Canine Multipotent Stromal Cells from Subcutaneous and Infrapatellar Adipose Tissue.. Stem Cell Rev Rep 2016 Apr;12(2):257-68.
- Duval K, Grover H, Han LH, Mou Y, Pegoraro AF, Fredberg J, Chen Z. Modeling Physiological Events in 2D vs. 3D Cell Culture.. Physiology (Bethesda) 2017 Jul;32(4):266-277.
- Eastham AM, Spencer H, Soncin F, Ritson S, Merry CL, Stern PL, Ward CM. Epithelial-mesenchymal transition events during human embryonic stem cell differentiation.. Cancer Res 2007 Dec 1;67(23):11254-62.
- Fonsatti E, Maio M. Highlights on endoglin (CD105): from basic findings towards clinical applications in human cancer.. J Transl Med 2004 Jun 11;2(1):18.
- French KR, Pollitt CC. Equine laminitis: loss of hemidesmosomes in hoof secondary epidermal lamellae correlates to dose in an oligofructose induction model: an ultrastructural study.. Equine Vet J 2004 Apr;36(3):230-5.
- Fülber J, Maria DA, da Silva LC, Massoco CO, Agreste F, Baccarin RY. Comparative study of equine mesenchymal stem cells from healthy and injured synovial tissues: an in vitro assessment.. Stem Cell Res Ther 2016 Mar 5;7:35.
- Galantino-Homer H. L., Clark R. K., Linardi R. L.. Characterization of equine hoof lamellar tissue microanatomy with fluorescent markers. Proceedings of the 60th Annual Convention of the American Association of Equine Practitioners Salt Lake City, UT: American Association of Equine Practitioners (AAEP), 73–78.
- Gallucci BB, Shulman HM, Sale GE, Lerner KG, Caldwell LE, Thomas ED. The ultrastructure of the human epidermis in chronic graft-versus-host disease.. Am J Pathol 1979 Jun;95(3):643-62.
- Gargett CE, Schwab KE, Zillwood RM, Nguyen HP, Wu D. Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium.. Biol Reprod 2009 Jun;80(6):1136-45.
- Gerhard DS, Wagner L, Feingold EA, Shenmen CM, Grouse LH, Schuler G, Klein SL, Old S, Rasooly R, Good P, Guyer M, Peck AM, Derge JG, Lipman D, Collins FS, Jang W, Sherry S, Feolo M, Misquitta L, Lee E, Rotmistrovsky K, Greenhut SF, Schaefer CF, Buetow K, Bonner TI, Haussler D, Kent J, Kiekhaus M, Furey T, Brent M, Prange C, Schreiber K, Shapiro N, Bhat NK, Hopkins RF, Hsie F, Driscoll T, Soares MB, Casavant TL, Scheetz TE, Brown-stein MJ, Usdin TB, Toshiyuki S, Carninci P, Piao Y, Dudekula DB, Ko MS, Kawakami K, Suzuki Y, Sugano S, Gruber CE, Smith MR, Simmons B, Moore T, Waterman R, Johnson SL, Ruan Y, Wei CL, Mathavan S, Gunaratne PH, Wu J, Garcia AM, Hulyk SW, Fuh E, Yuan Y, Sneed A, Kowis C, Hodgson A, Muzny DM, McPherson J, Gibbs RA, Fahey J, Helton E, Ketteman M, Madan A, Rodrigues S, Sanchez A, Whiting M, Madari A, Young AC, Wetherby KD, Granite SJ, Kwong PN, Brinkley CP, Pearson RL, Bouffard GG, Blakesly RW, Green ED, Dickson MC, Rodriguez AC, Grimwood J, Schmutz J, Myers RM, Butterfield YS, Griffith M, Griffith OL, Krzywinski MI, Liao N, Morin R, Palmquist D, Petrescu AS, Skalska U, Smailus DE, Stott JM, Schnerch A, Schein JE, Jones SJ, Holt RA, Baross A, Marra MA, Clifton S, Makowski KA, Bosak S, Malek J. The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC).. Genome Res 2004 Oct;14(10B):2121-7.
- Ghasemi N.. Comparison of two protocols for induction of differentiation of human adipose derived stem cells into oligodendrocyte progenitor cells. Sci. J. Kurdistan Univ. Med. Sci. 22, 93–102.
- Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo.. Proc Natl Acad Sci U S A 2000 Dec 5;97(25):13625-30.
- Gross T. L., Ihrke P. J., Walder E. J., Affolter V. K.. Skin Diseases of the Dog and Cat: Clinical and Histopathologic Diagnosis, 2nd Edn. Wiley .
- Halfon S, Abramov N, Grinblat B, Ginis I. Markers distinguishing mesenchymal stem cells from fibroblasts are downregulated with passaging.. Stem Cells Dev 2011 Jan;20(1):53-66.
- Hashimoto K. The ultrastructure of the skin of human embryos. X. Merkel tactile cells in the finger and nail.. J Anat 1972 Jan;111(Pt 1):99-120.
- Hayashi R, Ishikawa Y, Sasamoto Y, Katori R, Nomura N, Ichikawa T, Araki S, Soma T, Kawasaki S, Sekiguchi K, Quantock AJ, Tsujikawa M, Nishida K. Co-ordinated ocular development from human iPS cells and recovery of corneal function.. Nature 2016 Mar 17;531(7594):376-80.
- Horstmann H, Ng CP, Tang BL, Hong W. Ultrastructural characterization of endoplasmic reticulum--Golgi transport containers (EGTC).. J Cell Sci 2002 Nov 15;115(Pt 22):4263-73.
- Hunt RJ, Wharton RE. Clinical presentation, diagnosis, and prognosis of chronic laminitis in North America.. Vet Clin North Am Equine Pract 2010 Apr;26(1):141-53.
- Hwang GW, Murai Y, Takahashi T, Naganuma A. The protein transportation pathway from Golgi to vacuoles via endosomes plays a role in enhancement of methylmercury toxicity.. Sci Rep 2014 Jul 30;4:5888.
- Jiang T, Xu G, Wang Q, Yang L, Zheng L, Zhao J, Zhang X. In vitro expansion impaired the stemness of early passage mesenchymal stem cells for treatment of cartilage defects.. Cell Death Dis 2017 Jun 1;8(6):e2851.
- Johnson PJ, Tyagi SC, Katwa LC, Ganjam VK, Moore LA, Kreeger JM, Messer NT. Activation of extracellular matrix metalloproteinases in equine laminitis.. Vet Rec 1998 Apr 11;142(15):392-6.
- Khojasteh A, Fahimipour F, Jafarian M, Sharifi D, Jahangir S, Khayyatan F, Baghaban Eslaminejad M. Bone engineering in dog mandible: Coculturing mesenchymal stem cells with endothelial progenitor cells in a composite scaffold containing vascular endothelial growth factor.. J Biomed Mater Res B Appl Biomater 2017 Oct;105(7):1767-1777.
- Kisiday J, Jin M, Kurz B, Hung H, Semino C, Zhang S, Grodzinsky AJ. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair.. Proc Natl Acad Sci U S A 2002 Jul 23;99(15):9996-10001.
- Koerner J, Nesic D, Romero JD, Brehm W, Mainil-Varlet P, Grogan SP. Equine peripheral blood-derived progenitors in comparison to bone marrow-derived mesenchymal stem cells.. Stem Cells 2006 Jun;24(6):1613-9.
- Kummer M, Lischer C, Ohlerth S, Vargas J, Auer J. Evaluation of a standardised radiographic technique of the equine hoof.. Schweiz Arch Tierheilkd 2004 Nov;146(11):507-14.
- Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition.. Nat Rev Mol Cell Biol 2014 Mar;15(3):178-96.
- Leise BS, Faleiros RR, Watts M, Johnson PJ, Black SJ, Belknap JK. Laminar inflammatory gene expression in the carbohydrate overload model of equine laminitis.. Equine Vet J 2011 Jan;43(1):54-61.
- Leung Y, Kandyba E, Chen YB, Ruffins S, Chuong CM, Kobielak K. Bifunctional ectodermal stem cells around the nail display dual fate homeostasis and adaptive wounding response toward nail regeneration.. Proc Natl Acad Sci U S A 2014 Oct 21;111(42):15114-9.
- Lian JB, Stein GS. Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation.. Crit Rev Oral Biol Med 1992;3(3):269-305.
- Liao Y, Itoh M, Yang A, Zhu H, Roberts S, Highet AM, Latshaw S, Mitchell K, van de Ven C, Christiano A, Cairo MS. Human cord blood-derived unrestricted somatic stem cells promote wound healing and have therapeutic potential for patients with recessive dystrophic epidermolysis bullosa.. Cell Transplant 2014 Mar;23(3):303-17.
- Linardi RL, Megee SO, Mainardi SR, Senoo M, Galantino-Homer HL. Expression and localization of epithelial stem cell and differentiation markers in equine skin, eye and hoof.. Vet Dermatol 2015 Aug;26(4):213-e47.
- Lombana KG, Goodrich LR, Phillips JN, Kisiday JD, Ruple-Czerniak A, McIlwraith CW. An Investigation of Equine Mesenchymal Stem Cell Characteristics from Different Harvest Sites: More Similar Than Not.. Front Vet Sci 2015;2:67.
- Longland AC, Byrd BM. Pasture nonstructural carbohydrates and equine laminitis.. J Nutr 2006 Jul;136(7 Suppl):2099S-2102S.
- Maiolino S. A., Kingston A. K., Lemelin P.. Comparative and functional morphology of the primate hand integument. The Evolution of the Primate Hand. Developments in Primatology: Progress and Prospects New York, NY: Springer.
- Martins L., Valente F., Reis E., Sepúlveda R., Perdigão A., Borges A.. Treatment of periodontal disease with guided tissue regeneration technique using a hydroxyapatite and polycaprolactone membrane. Arq. Bras. Med. Vet. Zootec. 68, 1413–1421.
- Matic I, Antunovic M, Brkic S, Josipovic P, Mihalic KC, Karlak I, Ivkovic A, Marijanovic I. Expression of OCT-4 and SOX-2 in Bone Marrow-Derived Human Mesenchymal Stem Cells during Osteogenic Differentiation.. Open Access Maced J Med Sci 2016 Mar 15;4(1):9-16.
- McCarthy HE, Bara JJ, Brakspear K, Singhrao SK, Archer CW. The comparison of equine articular cartilage progenitor cells and bone marrow-derived stromal cells as potential cell sources for cartilage repair in the horse.. Vet J 2012 Jun;192(3):345-51.
- Medvedev SP, Malakhova AA, Grigor'eva EV, Shevchenko AI, Dementyeva EV, Sobolev IA, Lebedev IN, Shilov AG, Zhimulev IF, Zakian SM. Derivation of induced pluripotent stem cells from fetal human skin fibroblasts.. Acta Naturae 2010 Jul;2(2):102-6.
- Michel M, Török N, Godbout MJ, Lussier M, Gaudreau P, Royal A, Germain L. Keratin 19 as a biochemical marker of skin stem cells in vivo and in vitro: keratin 19 expressing cells are differentially localized in function of anatomic sites, and their number varies with donor age and culture stage.. J Cell Sci 1996 May;109 ( Pt 5):1017-28.
- Miko M, Danišovič L, Majidi A, Varga I. Ultrastructural analysis of different human mesenchymal stem cells after in vitro expansion: a technical review.. Eur J Histochem 2015 Oct 26;59(4):2528.
- Miragliotta V, Donadio E, Felicioli A, Podestà A, Ricciardi MP, Ceccardi S, Abramo F. Immunolocalisation of desmoglein-1 in equine muzzle skin.. Equine Vet J 2006 Sep;38(5):485-7.
- Morgan SJ, Grosenbaugh DA, Hood DM. The pathophysiology of chronic laminitis. Pain and anatomic pathology.. Vet Clin North Am Equine Pract 1999 Aug;15(2):395-417, vii.
- Morrison S., Dryden V. C., Bras R., Morrell S.. How to use stem cells in clinical laminitis cases. Proceedings of the 60th Annual Convention of the American Association of Equine Practitioners Salt Lake City, UT: American Association of Equine Practitioners (AAEP), 499–503.
- Najor NA. Desmosomes in Human Disease.. Annu Rev Pathol 2018 Jan 24;13:51-70.
- Nourian AR, Baldwin GI, van Eps AW, Pollitt CC. Equine laminitis: ultrastructural lesions detected 24-30 hours after induction with oligofructose.. Equine Vet J 2007 Jul;39(4):360-4.
- O'grady S. E.. White line disease - an update equine veterinary education. Equine Vet. Educ. 14, 51–55.
- Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. A summary of current work.. Lab Invest 1976 Mar;34(3):235-49.
- Paschos NK, Brown WE, Eswaramoorthy R, Hu JC, Athanasiou KA. Advances in tissue engineering through stem cell-based co-culture.. J Tissue Eng Regen Med 2015 May;9(5):488-503.
- Pascucci L, Mercati F, Marini C, Ceccarelli P, Dall'Aglio C, Pedini V, Gargiulo AM. Ultrastructural morphology of equine adipose-derived mesenchymal stem cells.. Histol Histopathol 2010 Oct;25(10):1277-85.
- Pearton DJ, Yang Y, Dhouailly D. Transdifferentiation of corneal epithelium into epidermis occurs by means of a multistep process triggered by dermal developmental signals.. Proc Natl Acad Sci U S A 2005 Mar 8;102(10):3714-9.
- Peroni J.. Regenerative medicine and laminitis: where are we?. J. Equine Vet. Sci. 33, 865–866.
- Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair--current views.. Stem Cells 2007 Nov;25(11):2896-902.
- Pollitt C. C.. Clinical anatomy and physiology of the normal equine foot equine veterinary education. Equine Vet. Educ. 4, 219–224.
- Pollitt CC. The basement membrane at the equine hoof dermal epidermal junction.. Equine Vet J 1994 Sep;26(5):399-407.
- Pollitt C. C.. The anatomy and physiology of the hoof wall. Equine Vet. Educ. 10, 318–325.
- Pollitt C. C.. Lamellar function at the cellular level. Equ. Lamin. 22–38.
- Pollitt CC, Daradka M. Equine laminitis basement membrane pathology: loss of type IV collagen, type VII collagen and laminin immunostaining.. Equine Vet J Suppl 1998 Sep;(26):139-44.
- Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators.. Nat Rev Mol Cell Biol 2003 Jan;4(1):33-45.
- Qi Y, Du Y, Li W, Dai X, Zhao T, Yan W. Cartilage repair using mesenchymal stem cell (MSC) sheet and MSCs-loaded bilayer PLGA scaffold in a rabbit model.. Knee Surg Sports Traumatol Arthrosc 2014 Jun;22(6):1424-33.
- Raimondo S, Penna C, Pagliaro P, Geuna S. Morphological characterization of GFP stably transfected adult mesenchymal bone marrow stem cells.. J Anat 2006 Jan;208(1):3-12.
- Ramírez GA, Rodríguez F, Herráez P, Castro-Alonso A, Andrada M, Espinosa-de-los-Monteros A. Ultrastructural characterization of normal Merkel cells in the dog.. Vet Dermatol 2015 Oct;26(5):328-33, e68-9.
- Ranera B, Lyahyai J, Romero A, Vázquez FJ, Remacha AR, Bernal ML, Zaragoza P, Rodellar C, Martín-Burriel I. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue.. Vet Immunol Immunopathol 2011 Nov 15;144(1-2):147-54.
- Rodrigues G. C., Oliveira L. J., Monteiro J. M., De Lima A. R., Gonçalez P. O., Hernandez-Blazquez F. J.. Ultrastructural characterization of bovine umbilical cord blood cells. Pesqui. Vet. Bras. 30, 897–902.
- Rohani N, Canty L, Luu O, Fagotto F, Winklbauer R. EphrinB/EphB signaling controls embryonic germ layer separation by contact-induced cell detachment.. PLoS Biol 2011 Mar;9(3):e1000597.
- Rucker A. Chronic laminitis: strategic hoof wall resection.. Vet Clin North Am Equine Pract 2010 Apr;26(1):197-205.
- Rustad KC, Wong VW, Sorkin M, Glotzbach JP, Major MR, Rajadas J, Longaker MT, Gurtner GC. Enhancement of mesenchymal stem cell angiogenic capacity and stemness by a biomimetic hydrogel scaffold.. Biomaterials 2012 Jan;33(1):80-90.
- Saito M, Tucker DK, Kohlhorst D, Niessen CM, Kowalczyk AP. Classical and desmosomal cadherins at a glance.. J Cell Sci 2012 Jun 1;125(Pt 11):2547-52.
- Sardarabadi P., Soleimani M., Atashi A., Beiranvand S. P., Rahnama M. A., Anbarlou A.. Gene expression analysis of SOX2, NANOG, KLF4, OCT4, and REX1 genes in cord blood mononuclear cells treated with external stresses. Int. J. Health Stud. 2, 10–13.
- Schäffler A, Büchler C. Concise review: adipose tissue-derived stromal cells--basic and clinical implications for novel cell-based therapies.. Stem Cells 2007 Apr;25(4):818-27.
- Senoo M, Pinto F, Crum CP, McKeon F. p63 Is essential for the proliferative potential of stem cells in stratified epithelia.. Cell 2007 May 4;129(3):523-36.
- Shokrgozar MA, Fattahi M, Bonakdar S, Ragerdi Kashani I, Majidi M, Haghighipour N, Bayati V, Sanati H, Saeedi SN. Healing potential of mesenchymal stem cells cultured on a collagen-based scaffold for skin regeneration.. Iran Biomed J 2012;16(2):68-76.
- Smoak M., Hogan K., Kriegh L., Chen C., Terrell L. B., Qureshi A. T.. Modulation of mesenchymal stem cell behavior by nano-and micro-sized β-tricalcium phosphate particles in suspension and composite structures. J. Nanopart. Res. 17:182.
- Sotiropoulou PA, Perez SA, Salagianni M, Baxevanis CN, Papamichail M. Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells.. Stem Cells 2006 Feb;24(2):462-71.
- Sun TT, Green H. Differentiation of the epidermal keratinocyte in cell culture: formation of the cornified envelope.. Cell 1976 Dec;9(4 Pt 1):511-21.
- Sundelacruz S, Kaplan DL. Stem cell- and scaffold-based tissue engineering approaches to osteochondral regenerative medicine.. Semin Cell Dev Biol 2009 Aug;20(6):646-55.
- Takahashi H, Shimizu T, Nakayama M, Yamato M, Okano T. The use of anisotropic cell sheets to control orientation during the self-organization of 3D muscle tissue.. Biomaterials 2013 Oct;34(30):7372-80.
- Thomason HA, Scothern A, McHarg S, Garrod DR. Desmosomes: adhesive strength and signalling in health and disease.. Biochem J 2010 Aug 1;429(3):419-33.
- Tomasello L, Mauceri R, Coppola A, Pitrone M, Pizzo G, Campisi G, Pizzolanti G, Giordano C. Mesenchymal stem cells derived from inflamed dental pulpal and gingival tissue: a potential application for bone formation.. Stem Cell Res Ther 2017 Aug 1;8(1):179.
- Troy TC, Arabzadeh A, Turksen K. Re-assessing K15 as an epidermal stem cell marker.. Stem Cell Rev Rep 2011 Nov;7(4):927-34.
- Van Eps AW, Pollitt CC. Equine laminitis model: lamellar histopathology seven days after induction with oligofructose.. Equine Vet J 2009 Nov;41(8):735-40.
- Vidal MA, Kilroy GE, Lopez MJ, Johnson JR, Moore RM, Gimble JM. Characterization of equine adipose tissue-derived stromal cells: adipogenic and osteogenic capacity and comparison with bone marrow-derived mesenchymal stromal cells.. Vet Surg 2007 Oct;36(7):613-22.
- Vidal MA, Walker NJ, Napoli E, Borjesson DL. Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue.. Stem Cells Dev 2012 Jan 20;21(2):273-83.
- Violini S, Ramelli P, Pisani LF, Gorni C, Mariani P. Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12.. BMC Cell Biol 2009 Apr 22;10:29.
- Visser MB, Pollitt CC. Characterization of extracellular matrix macromolecules in primary cultures of equine keratinocytes.. BMC Vet Res 2010 Mar 15;6:16.
- Visser MB, Pollitt CC. Immunohistochemical distribution of laminin-332 and collagen type IV in the basement membrane of normal horses and horses with induced laminitis.. J Comp Pathol 2011 Jul;145(1):80-7.
- Walko G, Castañón MJ, Wiche G. Molecular architecture and function of the hemidesmosome.. Cell Tissue Res 2015 Jun;360(3):529-44.
- Xie L, Zhang N, Marsano A, Vunjak-Novakovic G, Zhang Y, Lopez MJ. In vitro mesenchymal trilineage differentiation and extracellular matrix production by adipose and bone marrow derived adult equine multipotent stromal cells on a collagen scaffold.. Stem Cell Rev Rep 2013 Dec;9(6):858-72.
- Zhang N, Dietrich MA, Lopez MJ. Canine intra-articular multipotent stromal cells (MSC) from adipose tissue have the highest in vitro expansion rates, multipotentiality, and MSC immunophenotypes.. Vet Surg 2013 Feb;42(2):137-46.
- Zhang N, Dietrich MA, Lopez MJ. Therapeutic doses of multipotent stromal cells from minimal adipose tissue.. Stem Cell Rev Rep 2014 Aug;10(4):600-11.
- Zheng Y, Hu CJ, Zhuo RH, Lei YS, Han NN, He L. Inhibition of autophagy alleviates the senescent state of rat mesenchymal stem cells during long-term culture.. Mol Med Rep 2014 Dec;10(6):3003-8.
- Zhou X, Xiang Y, Ding X, Garrard WT. Loss of an Igκ gene enhancer in mature B cells results in rapid gene silencing and partial reversible dedifferentiation.. Mol Cell Biol 2013 May;33(10):2091-101.
Citations
This article has been cited 3 times.- Pielok A, Kępska M, Steczkiewicz Z, Grobosz S, Bourebaba L, Marycz K. Equine Hoof Progenitor Cells Display Increased Mitochondrial Metabolism and Adaptive Potential to a Highly Pro-Inflammatory Microenvironment.. Int J Mol Sci 2023 Jul 14;24(14).
- Watanabe M, Ida Y, Ohguro H, Ota C, Hikage F. Establishment of appropriate glaucoma models using dexamethasone or TGFβ2 treated three-dimension (3D) cultured human trabecular meshwork (HTM) cells.. Sci Rep 2021 Sep 29;11(1):19369.
- Hisey E, Ross PJ, Meyers SA. A Review of OCT4 Functions and Applications to Equine Embryos.. J Equine Vet Sci 2021 Mar;98:103364.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists