Spermatogonial SOHLH1 nucleocytoplasmic shuttling associates with initiation of spermatogenesis in the rhesus monkey (Macaca mulatta)

Molecular Human Reproduction

Volumn 20, Issue 4, 2014, Pages 350-357

  Ramaswamy, Suresh ^a,b   Razack, Bibi S ^c   Roslund, Rachel M ^a   Suzuki, Hitomi ^a   Marshall, Gary R ^c   Rajkovic, Aleksandar ^a,b   Plant, Tony M ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CHATHAM UNIVERSITY   (United States)

Author keywords

Rhesus monkey; SOHLH1; Spermatogenesis; Spermatogonial differentiation

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR ALPHA 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOHLH1; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GERM CELL; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RHESUS MONKEY; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS; TESTIS DEVELOPMENT; UPREGULATION;

RHESUS MONKEY; SOHLH1; SPERMATOGENESIS; SPERMATOGONIAL DIFFERENTIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; MACACA MULATTA; MALE; PROTO-ONCOGENE PROTEINS C-KIT; SEXUAL MATURATION; SPERMATOGENESIS; SPERMATOGONIA; TESTIS;

EID: 84896467017     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat093     Document Type: Article

References (31)

1. Ahmed EA, de Rooij DG. Staging of mouse seminiferous tubule cross-sections. Methods Mol Biol 2009;558:263-277.
2. Amann RP. The cycle of the seminiferous epithelium in humans: a need to revisit? J Androl 2008;29:469-487.
3. Aponte PM, van Bragt MPA, de Rooij DG, van Pelt AMM. Spermatogonial stem cells: characteristics and experimental possibilities. APMIS 2005; 113:727-742.
4. Ballow D, Meistrich ML, Matzuk MM, Rajkovic A. Sohlh1 is essential for spermatogonial differentiation. Dev Biol 2006;294:161-167.
5. Barrios F, Filipponi D, Campolo F, Gori M, Bramucci F, Pellegrini M, Ottolenghi S, Rossi P, Jannini EA, Dolci S. SOHLH1 and SOHLH2 control Kit expression during postnatal male germ cell development. J Cell Sci 2012;125:1455-1464.
6. Choi Y, Jeon S, Choi M, Lee MH, Park M, Lee DR, Jun KY, Kwon Y, Lee OH, Song SH et al. Mutations in SOHLH1 gene associate with nonobstructive azoospermia. Hum Mutat 2010;31:788-793.
7. Clermont Y. Kinetics of spermatogenesis inmammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972;52:198-236.
8. De Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000;21:776-798.
9. Ehmcke J, Luetjens CM, Schlatt S. Clonal organization of proliferating spermatogonial cells in adult males of two species of non-human primates, Macaca mulattta and Callithrix jacchus. Biol Reprod 2005;72:293-300.
10. Gassei K, Ehmcke J, Dhir R, Schlatt S. Magnetic activated cell sorting allows isolation of spermatogonia from adult primate testes and reveals distinct GFRa1-positive subpopulation in men. J Med Primatol 2010;39:83-91.
11. Hao J, Yamamoto M, Richardson TE, Chapman KM, Denard BS,Hammer RE, Zhao GQ, Hamra FK. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008; 26:1587-1597.
12. Hermann BP, Sukhwani M, Simorangkir DR, Chu T, Plant TM, Orwig KE. Molecular dissection of the male germ cell lineage identifies putative spermatogonial stem cells in rhesus macaques. Hum Reprod 2009; 24:1704-1716.
13. Hermann BP, Sukhwani M, Hansel MC, Orwig KE. Spermatogonial stem cells in higher primates: are there differences from those in rodents? Reproduction 2010;139:479-493.
14. Luetjens CM, Weinbauer GF, Wistuba J. Primate spermatogenesis: new insights into comparative testicular organization, spermatogenic efficiency and endocrine control. Biol Rev 2005;80:475-488.
15. Marshall GR, Plant TM. Puberty occurring either spontaneously or induced precociously in rhesus monkey (Macaca mulatta) is associated with a marked proliferation of Sertoli cells. Biol Reprod 1996;54:1192-1199.
16. Marshall GR, Ramaswamy S, Plant TM. Gonadotropin-independent proliferation of the pale type A spermatogonia in the adult rhesus monkey (Macaca mulatta). Biol Reprod 2005;73:222-229.
17. Mauduit C, Hamamah S, Benahmed M. Stem cell factor/c-kit system in spermatogenesis. Hum Reprod Update 1999;5:535-545.
18. Muciaccia B, Boitani C, Berloco P, Nudo F, Spadetta G, Stefanini M, de Rooij DG, Vicini E. Novel stage classification of human spermatogenesis based on acrosome development. Biol Repro 2013. doi:10.1095/ biolreprod.113.111682.
19. Plant TM. A study of the role of the postnatal testes in determining the ontogeny of gonadotropin secretion in the male rhesus monkey (Macaca mulatta). Endocrinology 1985;116:1341-1350.
20. Plant TM. Undifferentiated primate spermatogonia and their endocrine control. Trends Endocrinol and Metab 2010;21:488-495.
21. Plant TM, Witchel SF. Puberty in non-human primates and humans. In: Challis JRG, de Kretser DM, Neill JD, Pfaff DW, Plant TM, Richards JS, Wasserman PM (eds). Knobil and Neill's Physiology of Reproduction. San Diego, CA, USA: Elsevier, 2006, 2177-2230.
22. Plant TM, Ramaswamy S, Simorangkir DR, Marshall GR. Postnatal and pubertal development of the rhesus monkey (Macaca mulatta) testis. Ann NY Acad Sci 2005;1061:149-162.
23. Ramaswamy S, Plant TM, Marshall GR. Pulsatile stimulation with recombinant single chain human luteinizing hormone elicits precocious Sertoli cell proliferation in the juvenile male rhesus monkey (Macaca mulatta). Biol Reprod 2000;63:82-88.
24. Ramaswamy S, Seminara SB, Pohl CR, DiPietro MJ,CrowleyWFJr., Plant TM. Effect of continuous intravenous administration of human metastin 45-54 on the neuroendocrine activity of the hypothalamic-pituitary-testicular axis in the adult male rhesus monkey (Macaca mulatta). Endocrinology 2007;148:3364-3370.
25. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM. Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology 2008;149: 4387-4395.
26. Simorangkir DR, Marshall GR, Ehmcke J, Schlatt S, Plant TM. Prepubertal expansion of dark and pale type A spermatogonia in the rhesus monkey (Macaca mulatta) results from proliferation during infantile and juvenile development in a relatively gonadotropin independent manner. Biol Reprod 2005;73:1109-1115.
27. Simorangkir DR, Marshall GR, Plant TM. A re-examination of proliferation and differentiation of type A spermatogonia in the adult rhesus monkey (Macaca mulatta). Human Reprod 2009;24:1596-1604.
28. Simorangkir DR, Ramaswamy S, Marshall GR, Roslund R, Plant TM. Sertoli cell differentiation in rhesus monkey (Macaca mulatta) is an early event in puberty and precedes attainment of the adult complement of undifferentiated spermatogonia. Reproduction 2012;143:513-522.
29. Suzuki H, Ahn HW, Chu T, Bowden W, Gassei K, Orwig K, Rajkovic A. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Dev Biol 2012;361:301-312.
30. Toyoda S, Miyazaki T, Miyazaki S, Yoshimura T, Yamamoto M, Tashiro F, Yamato E, Miyazaki J. Sohlh2 affects differentiation of KIT positive oocytes and spermatogonia. Dev Biol 2009;325:238-248.
31. Tsuneyoshi N, Dunn NR. Guards at the gate to embryonic stem cell differentiation. Cell 2013;153:281-283.