Ontogeny of the Kidney and Renal Developmental Markers in the Rhesus Monkey (Macaca Mulatta)

Anatomical Record

Volumn 293, Issue 11, 2010, Pages 1971-1983

  Batchelder, Cynthia A ^a   Lee, C Chang I ^a   Martinez, Michele L ^a   Tarantal, Alice F ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Kidney; Nephrogenesis; Nestin; Ontogeny; Pax2; Progenitors; WT1

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BIOLOGICAL MARKER; CD31 ANTIGEN; NESTIN; SYNAPTOPODIN; TRANSCRIPTION FACTOR PAX2; VASCULOTROPIN; WT1 PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL POPULATION; EMBRYONIC STEM CELL; GENE EXPRESSION; GLOMERULUS; IMMUNOHISTOCHEMISTRY; KIDNEY DEVELOPMENT; KIDNEY PARENCHYMA; MACACA; MESANGIUM CELL; NONHUMAN; ONTOGENY; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUALITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SECOND TRIMESTER PREGNANCY; TISSUE ENGINEERING; TISSUE REPAIR; UPREGULATION;

ACTINS; ANIMALS; ANTIGENS, CD31; BIOLOGICAL MARKERS; ENDOTHELIUM; FEMALE; FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERMEDIATE FILAMENT PROTEINS; KIDNEY; KIDNEY GLOMERULUS; MACACA MULATTA; NERVE TISSUE PROTEINS; PAX2 TRANSCRIPTION FACTOR; PREGNANCY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WT1 PROTEINS;

MACACA MULATTA; PRIMATES;

EID: 78049474955     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21242     Document Type: Article

References (51)

1. Agrawal R, Tran U, Wessely O. 2008. Expression and functional analysis of miRNAs in kidney development. Dev Biol 319: 605. doi:10.1016/jmydbio.2008.05.447.
2. Agrawal R, Tran U, Wessely O. 2009. The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development 136: 3927-3936.
3. Appel D, Kershaw DB, Smeets B, Yan G, Fuss A, Frye B, Elger M, Kriz W, Floege J, Moeller MJ. 2009. Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol 20: 333-343.
4. Armstrong JF, Pritchard-Jones K, Bickmore WA, Hastie ND, Bard JBL. 1992. The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech Dev 40: 85-97.
5. Batchelder CA, Lee CCI, Matsell DG, Yoder MC, Tarantal AF. 2009. Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors. Differentiation 78: 45-56.
6. Barisoni L, Mokrzycki M, Sablay L, Nagata M, Yamase H, Mundel P. 2000. Podocyte cell cycle regulation and proliferation in collapsing glomerulopathies. Kidney Int 58: 137-143.
7. Bertelli E, Regloi M, Fonzi L, Occhini R, Mannucci S, Ermini L, Toti P. 2007. Nestin expression in adult and developing human kidney. J Histochem Cytochem 55: 411-421.
8. Bontrop RE. 2001. Non-human primates: essential partners in biomedical research. Immunol Rev 183: 5-9.
9. Boyle S, Misfeldt A, Chandler KJ, Deal KK, Southard-Smith EM, Mortlock DP, Baldwin HS, de Caestecker M. 2008. Fate mapping using Cited1-CreERT2 mice demonstrates that the cap mesenchyme contains self-renewing progenitor cells and gives rise exclusively to nephronic epithelia. Dev Biol 313: 234-245.
10. Butt MJ, Tarantal AF, Jimenez DF, Matsell DG. 2007. Collecting duct epithelial-mesenchymal transition in fetal urinary tract obstruction. Kidney Int 72: 936-944.
11. Charles AK, Mall S, Watson J, Berry PJ. 1997. Expression of the Wilms' tumour gene WT1 in the developing human and in paediatric renal tumours: an immunohistochemical study. J Clin Pathol: Mol Pathol 50: 138-144.
12. Chen J, Boyle S, Zhao M, Su W, Takahashi K, Davis L, DeCaestecker M, Takahashi T, Breyer MD, Haeo C-M. 2006. Differential expression of the intermediate filament protein nestin during renal development and its localization in adult podocytes. J Am Soc Nephrol 17: 1283-1291.
13. Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS. 2007. Prevalence of chronic kidney disease in the United States. JAMA 298: 2038-2047.
14. Dressler GR, Deutsch U, Chowdhury K, Nornes HO, Gruss P. 1990. Pax2, a new murine paired-box containing gene and its expression in the developing excretory system. Development 109: 787-795.
15. Dressler GR, Douglass EC. 1992. Pax-2 is a DNA-binding protein expressed in embryonic kidney and Wilms' tumor. Proc Natl Acad Sci USA 89: 1179-1183.
16. Georgas K, Rumballe B, Wilkinson L, Chiu HS, Lesieur E, Gilbert T, Little MH. 2008. Use of dual section mRNA in situ hybridization/immunohistochemistry to clarify gene expression patterns during the early stages of nephron development in the embryo and in the mature nephron of the adult mouse kidney. Histochem Cell Biol 130: 927-942.
17. Hiatt MJ, Ivanova L, Toran N, Tarantal AF, Matsell DG. 2010. Remodeling of the fetal collecting duct epithelium. Am J Pathol 176: 630-637.
18. Ivanova L, Hiatt MJ, Yoder MC, Tarantal AF, Matsell DG. 2010. Ontogeny of CD24 in the human kidney. Kidney Int. 77: 1123-1131.
19. Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP. 2008. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3: 169-181.
20. Lazzeri E, Crescioli C, Ronconi E, Mazzinghi B, Sagrinati C, Netti GS, Angelotti ML, Parente E, Ballerini L, Cosmi L, Maggi L, Gesualdo L, Rotondi M, Annunziato F, Maggi E, Lasagni L, Serio M, Romagnani S, Vannelli GB, Romagnani P. 2007. Regenerative potential of embryonic renal multipotent progenitors in acute renal failure. J Am Soc Nephrol 18: 3128-3138.
21. Leapley AC, Lee CC, Batchelder CA, Yoder MC, Matsell DG, Tarantal AF. 2009. Characterization and culture of fetal rhesus monkey renal cortical cells. Pediatr Res 66: 448-454.
22. Lee CI, Goldstein O, Han VKM, Tarantal AF. 2001. IGF-II and IGF binding protein (IGFBP-1, IGFBP-3) gene expression in fetal rhesus monkey tissues during the second and third trimesters. Pediatr Res 49: 379-387.
23. Little MH, Rae FK. 2009. Potential cellular therapies for renal disease: can we translate results from animal studies to the human condition? Nephrology 14: 544-553.
24. MacPherson BR, Leslie KO, Lizaso KV, Schwarz JE. 1993. Contractile cells of the kidney in primary glomerular disorders: an immunohistochemical study using an anti-alpha-smooth muscle actin monoclonal antibody. Hum Pathol 24: 710-716.
25. Matsell DG, Mok A, Tarantal AF. 2002. Altered primate glomerular development due to in utero urinary tract obstruction. Kidney Int 61: 1263-1269.
26. Matsell DG, Tarantal AF. 2002. Experimental models of fetal obstructive nephropathy. Pediatr Nephrol 17: 470-476.
27. McMahon R, Murphy M, Clarkson M, Taal M, Mackenzie HS, Godson C, Martin F, Brady HR. 2000. IHG-2, a mesangial cell gene induced by high glucose, is human gremlin. J Biol Chem 275: 9901-9904.
28. Mezquita P, Beard BC, Kiem HP. 2008. NOD/SCID repopulating cells contribute only to short-term repopulation in the baboon. Gene Ther 15: 1460-1462.
29. Mundel P, Gilbert P, Kriz W. 1991. Podocytes in glomerulus of rat kidney express a characteristic 44 kd protein. J Histochem Cytochem 39: 1047-1056.
30. Mundel P, Heid HW, Mundel TM, Krüger M, Reiser J, Kriz W. 1997. Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 139: 193-204.
31. Mundlos S, Pelletier J, Darveau A, Bachmann M, Winterpacht A, Zabel B. 1993. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119: 1329-1341.
32. Mugford JW, Sipilä P, McMahon JA, McMahon AP. 2008. Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev Biol 324: 88-98.
33. Nagata M, Nakayama K, Terada Y, Hoshi S, Watanabe T. 1998. Cell cycle regulation and differentiation in the human podocyte lineage. Am J Pathol 153: 1511-1520.
34. Naruse K, Fujieda M, Miyazaki E, Hayashi Y, Toi M, Fukui T, Kuroda N, Hiroi M, Kurashige T, Enzan H. 2000. An immunohistochemical study of developing glomeruli in human fetal kidneys. Kidney Int 57: 1836-1846.
35. Nirmalanandhan VS, Sittampalam GS. 2009. Stem cells in drug discovery, tissue engineering, and regenerative medicine: emerging opportunities and challenges. J Biomol Screen 14: 755-768.
36. Organ Procurement and Transplantation Network. 2008. Current US Waiting List by Organ, US DHHS. Available at: http://optn.transplant.hrsa.gov/latestData/rptData.asp
37. Pelletier J, Schalling M, Buckler AJ, Rogers A, Haber DA, Housman D. 1991. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev 5: 1345-1356.
38. Perara RJ. 2007. A microarray-based method to profile global microRNA expression in human and mouse. Methods Mol Biol 382: 137-148.
39. Pritchard-Jones K, Fleming S, Davidson D, Bickmore W, Porteous D, Gosden C, Bard J, Buckler A, Pelletier J, Housman D, van Heyningen V, Hastie N. 1990. The candidate Wilms' tumor gene is involved in genitourinary development. Nature 346: 194-197.
40. Rackley RR, Flenniken AM, Kuriyan NP, Kessler PM, Stoler MH, Williams BRG. 1993. Expression of the Wilms' Tumor suppressor gene WT1 during mouse embryogenesis. Cell Growth Diff 4: 1023-1031.
41. Rao PK, Palmer JS. 2009. Prenatal and postnatal management of hydronephrosis. Sci World J 13: 606-614.
42. Ronconi E, Sagrinati C, Angelotti ML, Lazzeri E, Mazzinghi B, Ballerini L, Parente E, Becherucci F, Gacci M, Carini M, Maggi E, Serio M, Vannelli GB, Lasagni L, Romagnani S, Romangnani P. 2009. Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 20: 322-332.
43. Ryan G, Steele-Perkins V, Morris JF, Rauscher FJ, Dressler GR. 1995. Repression of Pax-2 by WT1 during normal kidney development. Development 121: 867-875.
44. Sagrinati C, Netti GS, Mazzinghi B, Lazzeri E, Liotta F, Frosali F, Ronconi E, Meini C, Gacci M, Squecco R, Carini M, Gesualdo L, Francini F, Maggi E, Annunziato F, Lasagni L, Serio M, Romagnani S, Romagnani P. 2006. Isolation and characterization of multipotent progenitor cells from Bowman's capsule of adult human kidneys. J Am Soc Nephrol 17: 2443-2456.
45. Saxen L. 1987. Organogenesis of the kidney. In: Barlow PW, Green PB, White CC, editors. Developmental and Cell Biology Series. Vol. 19. Cambridge, UK: Cambridge University Press. p 1-171.
46. Sharma PM, Yang X, Bowman M, Roberts V, Sukumar S. 1992. Molecular cloning of rat Wilms' Tumor complementary DNA and a study of messenger RNA expression in the urogenital system and the brain. Cancer Res 52: 6407-6412.
47. Shively CA, Clarkson TB. 2009. The unique value of primate models in translational research. Am J Primatol 72: 715-721.
48. Tarantal AF. 2005. Ultrasound imaging in rhesus (Macaca mulatta) and long-tailed (Macaca fascicularis) macaques: reproductive and research applications. In: Wolfe-Coote S, editor. The laboratory primate. Amsterdam: Elsevier. p 317-351.
49. Tarantal AF, Han VK, Cochrum KC, Mok A, daSilva M, Matsell DG. 2001. Fetal rhesus monkey model of obstructive renal dysplasia. Kidney Int 59: 446-456.
50. Tellier A-L, Amiel J, Delezoide A-L, Audollent S, Augé J, Esnault D, Encha-Razavi F, Munnich A, Lyonnet S, Vekemans M, Attié-Bitach T. 2000. Expression of the PAX2 gene in human embryos and exclusion in the CHARGE syndrome. Am J Med Genet 93: 85-88.
51. Wagner N, Wagner K-D, Scholz H, Kirschner KM, Schedl A. 2006. Intermediate filament protein nestin is expressed in developing kidney and heart and might be regulated by the Wilms' tumor suppressor Wt1. Am J Physiol Reg Integr Comp Physiol 291: 779-787.