Cell and Tissue Research

, Volume 367, Issue 2, pp 311–338 | Cite as

Comprehensive histological and immunological studies reveal a novel glycoprotein hormone and thyrostimulin expressing proto-glycotrope in the sea lamprey pituitary

  • Timothy J. Marquis
  • Masumi Nozaki
  • Wayne Fagerberg
  • Stacia A. Sower
Regular Article

Abstract

In the adenohypophysis (anterior pituitary) of all gnathostomes, there are six tropic cell types: corticotropes, melanotropes, somatotropes, lactotropes, gonadotropes and thyrotropes; each cell type produces specific tropic hormones. In contrast, we report in this study that there are only four tropic cell types in the sea lamprey (Petromyzon marinus) adenohypophysis. We specifically focused on the cell types that produce the glycoprotein hormones (GpHs). The gnathostome adenohypophyseal GpHs are follicle-stimulating hormone (FSH), luteinizing hormone (LH), thyroid-stimulating hormone (TSH), and thyrostimulin. However, lampreys only have two heterodimeric adenohypophyseal GpHs consisting of unique α and β subunits, lamprey GpH (lGpH) (lGpA2/lGpHβ) and thyrostimulin (lGpA2/lGpB5). We used an array of histological techniques to determine the (co)-localization and (co)-expression of the lGpH and thyrostimulin subunits in the lamprey adenohypophysis at different life stages (larval, parasitic, adult) and to identify their synthesizing cell(s). The thyrostimulin subunits (lGpA2/lGpB5) were co-expressed throughout the adenohypophysis (larval, parasitic, and adult), while the GpH β-subunit (lGpHβ) exhibited localized distribution (adult); all three subunits were co-localized and co-expressed, suggesting that both GpHs are synthesized in the same cells, novel proto-glycotropes, in specific adenohypophyseal regions at different life stages. In summary, we provide the first comprehensive study using histology, transmission electron microscopy, in situ hybridization and immunohistochemistry that strongly supports further evidence for four definitive adenohypophyseal cell types in the lamprey, including: corticotropes, somatotropes, melanotropes, and the first identification of a novel proto-glycotrope. In addition, our studies show that there is developmental and region-specific co-localization and co-expression of lGpH and thyrostimulin in the lamprey adenohypophysis.

Keywords

Glycoprotein hormones Proto-glycotrope Sea lamprey pituitary Thyrostimulin ISH, FISH, IHC and TEM of lamprey pituitary cell types 

Supplementary material

441_2016_2502_Fig15_ESM.gif (34 kb)
Fig. S1

Dot blot analysis to test the specificity of GpA2, GpHβ and GpB5 riboprobes for in situ hybridization. There was no expression observed for the no-probe controls for GpA2 (GpA2: C1), GpHβ (GpHβ: C1), or GpB5 (GpB5: C1). There was specific expression for the antisense (AS) probes for GpA2, GpHβ and GpB5, against the respective complementary sense DNA strands (GpA2: AS; GpHβ: AS; GpB5: AS), respectively; and sense (S) probes for GpA2, GpHβ and GpB5, against the respective complementary antisense DNA strands (GpA2: S; GpHβ: S; GpB5: S). There was no cross-reactivity between: GpA2 AS probes and GpHβ DNA (GpA2: C2) or GpB5 DNA (GpA2: C3); GpHβ AS probes and GpA2 DNA (GpHβ: C2) or GpB5 DNA (GpHβ: C3); or GpB5 AS probes and GpA2 DNA (GpB5: C2) or GpHβ DNA (GpB5: C3). Black arrowheads indicate the expression. White asterisks indicate pencil-mark reference points. (GpA2 shared lamprey thyrostimulin and GpH alpha (α) subunit (lGpA2), GpB5 hormone-specific lamprey thyrostimulin beta (β) subunit (lGpB5), GpHβ hormone-specific lamprey GpH beta (β) subunit (lGpHβ), AS antisense, S sense). (GIF 34 kb)

441_2016_2502_MOESM1_ESM.tif (2.4 mb)
High Resolution Image (TIF 2448 kb)
441_2016_2502_Fig16_ESM.gif (243 kb)
Fig. S2

ISH: GpA2. Single-labeled chromogenic in situ hybridization for the common alpha (α) subunit, GpA2, of lamprey (l) adenohypophyseal glycoprotein hormone (GpH) (lGpH) and thyrostimulin in female ammocoete, female parasitic phase and adult female and male lamprey adenohypophyses. GpA2 was minimally expressed in the rostral pars distalis (RPD) (a, b), proximal pars distalis (PPD) (a, c) and pars intermedia (PI) (a, d) of female ammocoete lampreys; moderately expressed in the RPD (e, f), PPD (e, g) and PI (e, h) of female parasitic phase lampreys; and highly expressed in the RPD (i, j), dorsal (i, k) and ventral (i, m) PPD and PI (i, l) of adult female lampreys; and highly expressed in the RPD (n, o), dorsal (n, p) and ventral (n, r) PPD and PI (n, q) of adult male lampreys. Arrowheads indicate the regions of expression. Scale bars (a) 100 μm, (bd) 20 μm. l lamprey, GpH lamprey glycoprotein hormone (lGpH), GpA2 shared lamprey thyrostimulin and GpH alpha (α) subunit (lGpA2), GpB5 hormone-specific lamprey thyrostimulin beta (β) subunit (lGpB5), GpHβ hormone-specific lamprey GpH beta (β) subunit (lGpHβ), AH adenohypophysis (anterior pituitary), RPD rostral pars distalis (region of AH), PPD proximal pars distalis (region of AH), PI pars intermedia (region of AH), NH neurohypophysis (posterior pituitary), III third ventricle. (GIF 242 kb)

441_2016_2502_MOESM2_ESM.tif (13.5 mb)
High Resolution Image (TIF 13874 kb)
441_2016_2502_Fig17_ESM.gif (210 kb)
Fig. S3

ISH: GpHβ. Single-labeled chromogenic in situ hybridization for the hormone specific beta (β) subunit, GpHβ, of lamprey (l) adenohypophyseal glycoprotein hormone (GpH) (lGpH) in female ammocoete, female parasitic phase and adult female and male lamprey adenohypophyses. GpHβ was not expressed in female ammocoete lampreys (ad); was moderately expressed in the RPD (e, f), PPD (e, g) and PI (e, h) of female parasitic phase lampreys; minimally expressed in the RPD (i, j), moderately expressed in the dorsal (i, k) and ventral (i, m) PPD and PI (i, l) of adult female lampreys; and minimally expressed in the RPD (n, o) and dorsal PPD (n, p) and highly expressed in the ventral PPD (n, r) and PI (n, q) of adult male lampreys. Arrowheads indicate the regions of expression. Scale bars (a) 100 μm, (bd) 20 μm. For abbreviations, see Fig. S2. (GIF 209 kb)

441_2016_2502_MOESM3_ESM.tif (12.9 mb)
High Resolution Image (TIF 13172 kb)
441_2016_2502_Fig18_ESM.gif (252 kb)
Fig. S4

ISH: GpB5. Single-labeled chromogenic in situ hybridization for the hormone specific beta (β) subunit, GpB5, of thyrostimulin in female ammocoete, female parasitic phase and adult female and male lamprey adenohypophyses. GpB5 was minimally to moderately expressed in the RPD (a, b), PPD (a, c) and PI (a, d) of female ammocoete lampreys; moderately expressed in the RPD (e, f), PPD (e, g) and PI (e, h) of female parasitic phase lampreys; and highly expressed in the RPD (i, j), dorsal (i, k) and ventral (i, m) PPD and PI (i, l) of adult female and male lampreys. Arrowheads indicate the regions of expression. Scale bars (a) 100 μm, (bd) 20 μm. For abbreviations, see Fig. S2. (GIF 251 kb)

441_2016_2502_MOESM4_ESM.tif (13.5 mb)
High Resolution Image (TIF 13786 kb)
441_2016_2502_Fig19_ESM.gif (473 kb)
Fig. S5

FISH: GpA2/GpHβ. Dual-labeled fluorescent in situ hybridization of the alpha (α) subunit, GpA2 and beta (β) subunit, GpHβ, of lamprey (l) adenohypophyseal glycoprotein hormone (GpH) (lGpH) in female ammocoete, female parasitic phase and adult female and male lamprey adenohypophyses. GpA2 and GpHβ transcripts were not co-expressed in female ammocoete lampreys (a, b: b2, c: c2, d: d2); were highly co-expressed in the RPD (e, f: f2), moderately co-expressed in the PPD (e, g: g2) and highly co-expressed in the PI (e, h: h2) of female parasitic phase lampreys; moderately to highly co-expressed in the dorsal PPD (i, k: k2), moderately co-expressed in the ventral PPD (i, l: l2) and minimally co-expressed in the PI (i, m: m2) of adult female lampreys; and moderately co-expressed in the dorsal PPD (n, p: p2), moderately to highly co-expressed in the ventral PPD (n, q: q2) and highly co-expressed in the PI (n, r: r2) of adult male lampreys. Arrowheads indicate the regions of expression. Scale bars (a) 100 μm, (bd) 20 μm. For abbreviations, see Fig. S2. (GIF 472 kb)

441_2016_2502_MOESM5_ESM.tif (23.4 mb)
High Resolution Image (TIF 23942 kb)
441_2016_2502_Fig20_ESM.gif (466 kb)
Fig. S6

FISH: GpA2/GpB5). Dual-labeled fluorescent in situ hybridization of the alpha (α) subunit, GpA2 and beta (β) subunit, GpB5, of thyrostimulin in female ammocoete, female parasitic phase and adult female and male lamprey adenohypophyses. GpA2 and GpB5 transcripts were moderately co-expressed in the PI of female ammocoete lampreys (a, d: d2); highly co-expressed in the RPD (e, f: f2), PPD (e, g: g2) and PI (e, h: h2) of female parasitic phase lampreys; highly co-expressed in the RPD (i, j: j2), dorsal (i, k: k2) and ventral PPD (i, l: l2) and PI (i, m: m2) of adult female lampreys; and highly co-expressed in the RPD (n, o: o2), dorsal (n, p: p2) and ventral PPD (n, q: q2) and PI (n, r: r2) of adult male lampreys. Arrowheads indicate the regions of expression. Scale bars (a) 100 μm, (bd) 20 μm. For abbreviations, see Fig. S2. (GIF 465 kb)

441_2016_2502_MOESM6_ESM.tif (22 mb)
High Resolution Image (TIF 22504 kb)
441_2016_2502_Fig21_ESM.gif (496 kb)
Fig. S7

FISH/IHC: triple co-expression of GpA2, GpHβ and GpB5 in adult female and male. Triple-labeled fluorescent in situ hybridization (FISH) and immunohistochemistry (IHC) of thyrostimulin subunits (α: GpA2, β: GpB5) and glycoprotein hormone subunits (α: GpA2, β: GpHβ) in adult female and male lamprey adenohypophyses. By FISH, all of the thyrostimulin and GpH subunits, GpA2, GpB5 and GpHβ were triple co-expressed (light teal) only in the ventral PPD of the AH in adult female (a) and male (b) lampreys, magnified from adult female (Fig. 3 e: e2) and male (Fig. 4 e: e2) AH, respectively. By IHC, all of the thyrostimulin and GpH subunits, GpA2, GpB5 and GpHβ were triple co-expressed (dark gray-magenta) only in the ventral PPD of the AH in adult female (c) and male (d) lampreys, magnified from adult female (Fig. 7 e: e2) and male (Fig. 8 e: e2) AH, respectively. Arrowheads in merged and individual images indicate the regions of triple co-expression of the lGpH and thyrostimulin subunits, GpA2, GpHβ and GpB5. Scale bars (a) 100 μm, (bd) 20 μm. l lamprey, GpH lamprey glycoprotein hormone (lGpH), GpA2 shared lamprey thyrostimulin and GpH alpha (α) subunit (lGpA2), GpB5 hormone specific lamprey thyrostimulin beta (β) subunit (lGpB5), GpHβ hormone specific lamprey GpH beta (β) subunit (lGpHβ), AH adenohypophysis (anterior pituitary), RPD rostral pars distalis (region of AH), PPD proximal pars distalis (region of AH), PI pars intermedia (region of AH), NH neurohypophysis (posterior pituitary), III third ventricle. (GIF 496 kb)

441_2016_2502_MOESM7_ESM.tif (11.4 mb)
High Resolution Image (TIF 11641 kb)
441_2016_2502_MOESM8_ESM.docx (32 kb)
Table S1Summary table of the individual expression of GpA2, GpHβ and GpB5 by single-label chromogenic ISH and co-expression of lGpH subunits, GpA2/GpHβ and thyrostimulin subunits, GpA2/GpB5, by dual-label FISH in female ammocoete, female parasitic phase and adult female and male lampreys. l lamprey, GpH lamprey glycoprotein hormone (lGpH), GpA2 shared lamprey thyrostimulin and GpH alpha (α) subunit (lGpA2), GpB5 hormone specific lamprey thyrostimulin beta (β) subunit (lGpB5), GpHβ hormone specific lamprey GpH beta (β) subunit (lGpHβ), AH adenohypophysis (anterior pituitary), RPD rostral pars distalis (region of AH), PPD proximal pars distalis (region of AH), D dorsal PPD, V ventral PPD, PI pars intermedia (region of AH), + minimal expression, ++ moderate expression, +++ high expression, — no expression. (DOCX 32 kb)

References

  1. Bloom W, Fawcett D (1975) A textbook of histology. Saunders, Philadelphia, PAGoogle Scholar
  2. Bolduc TG, Sower SA (1992) Changes in brain gonadotropin-releasing hormone, plasma estradiol 17-beta, and progesterone during the final reproductive cycle of the female sea lamprey, Petromyzon marinus. J Exp Zool 264:55–63CrossRefPubMedGoogle Scholar
  3. Dores RM, Baron AJ (2011) Evolution of POMC: origin, phylogeny, posttranslational processing, and the melanocortins. Ann N Y Acad Sci 1220:34–48CrossRefPubMedGoogle Scholar
  4. Dos Santos S, Bardet C, Bertrand S, Escriva H, Habert D, Querat B (2009) Distinct expression patterns of glycoprotein hormone-alpha2 and -beta5 in a basal chordate suggest independent developmental functions. Endocrinology 150:3815–3822CrossRefPubMedGoogle Scholar
  5. Fahien CM, Sower SA (1990) Relationship between brain gonadotropin-releasing hormone and final reproductive period of the adult male sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 80:427–437CrossRefPubMedGoogle Scholar
  6. Ficele G, Heinig JA, Kawauchi H, Youson JH, Keeley FW, Wright GM (1998) Spatial and temporal distribution of proopiomelanotropin and proopiocortin mRNA during the life cycle of the sea lamprey: a qualitative and quantitative in situ hybridization study. Gen Comp Endocrinol 110:212–225CrossRefPubMedGoogle Scholar
  7. Forey P, Janvier P (1993) Agnathans and the origin of jawed vertebrates. Nature 361:129–134CrossRefGoogle Scholar
  8. Gorbman A (1983) Comparative endocrinology. Wiley, New YorkGoogle Scholar
  9. Green JD, Maxwell DS (1958) Comparative anatomy of the hypophysis and observations on the mechanism of neurosecretion. In: Gorbman A (ed) Comparative endocrinology; proceedings of the Columbia University symposium on comparative endocrinology. Wiley, New York, pp 368–392Google Scholar
  10. Hall JA, Decatur WA, Daukss DM, Hayes MK, Marquis TJ, Morin SJ, Kelleher TF, Sower SA (2013) Expression of three GnRH receptors in specific tissues in male and female sea lampreys Petromyzon marinus at three distinct life stages. Front Neurosci 7:88CrossRefPubMedPubMedCentralGoogle Scholar
  11. Hardisty MW, Potter IC (1971) The biology of lampreys. Academic, LondonGoogle Scholar
  12. Heinig JA, Keeley FW, Robson P, Sower SA, Youson JH (1995) The appearance of proopiomelanocortin early in vertebrate evolution: cloning and sequencing of POMC from a Lamprey pituitary cDNA library. Gen Comp Endocrinol 99:137–144CrossRefPubMedGoogle Scholar
  13. Holmes JAY, John H (1994) Fall condition factor and temperature influence the incidence of metamorphosis in sea lampreys, Petromyzon marinus. Can J Zool 72:1134–1140CrossRefGoogle Scholar
  14. Kawauchi H, Suzuki K, Itoh H, Swanson P, Naito N, Nagahama Y, Nozaki M, Nakai Y, Itoh S (1989) The duality of teleost gonadotropins. Fish Physiol Biochem 7:29–38CrossRefPubMedGoogle Scholar
  15. Kawauchi H, Suzuki K, Yamazaki T, Moriyama S, Nozaki M, Yamaguchi K, Takahashi A, Youson J, Sower SA (2002) Identification of growth hormone in the sea lamprey, an extant representative of a group of the most ancient vertebrates. Endocrinology 143:4916–4921CrossRefPubMedGoogle Scholar
  16. Nakanishi S, Inoue A, Kita T, Nakamura M, Chang AC, Cohen SN, Numa S (1979) Nucleotide sequence of cloned cDNA for bovine corticotropin-beta-lipotropin precursor. Nature 278:423–427CrossRefPubMedGoogle Scholar
  17. Norris DO, Carr JA (2013) Vertebrate endocrinology. Elsevier, AmsterdamGoogle Scholar
  18. Nozaki M (2008) The hagfish pituitary gland and its putative adenohypophysial hormones. Zool Sci 25:1028–1036CrossRefPubMedGoogle Scholar
  19. Nozaki M, Ominato K, Shimotani T, Kawauchi H, Youson JH, Sower SA (2008) Identity and distribution of immunoreactive adenohypophysial cells in the pituitary during the life cycle of sea lampreys, Petromyzon marinus. Gen Comp Endocrinol 155:403–412CrossRefPubMedGoogle Scholar
  20. Nozaki M, Ominato K, Takahashi A, Kawauchi H, Sower SA (1999) Possible gonadotropin cells in the lamprey pituitary: colocalization of mammalian LH-like immunoreactivity and glycoconjugate in adult sea lampreys (Petromyzon marinus). Gen Comp Endocrinol 113:23–31CrossRefPubMedGoogle Scholar
  21. Nozaki M, Takahashi A, Amemiya Y, Kawauchi H, Sower SA (1995) Distribution of lamprey adrenocorticotropin and melanotropins in the pituitary of the adult sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 98:147–156CrossRefPubMedGoogle Scholar
  22. Okada SL, Ellsworth JL, Durnam DM, Haugen HS, Holloway JL, Kelley ML, Lewis KE, Ren H, Sheppard PO, Storey HM, Waggie KS, Wolf AC, Yao LY, Webster PJ (2006) A glycoprotein hormone expressed in corticotrophs exhibits unique binding properties on thyroid-stimulating hormone receptor. Mol Endocrinol 20:414–425CrossRefPubMedGoogle Scholar
  23. Ominato K, Nozaki M (2002) Glycoconjugate profiles of adrenocorticotropic and melanotropic cells in the pituitary of adult sea lampreys (Petromyzon marinus): a lectin histochemical study. Zool Sci 19:773–779CrossRefPubMedGoogle Scholar
  24. Paluzzi JP, Vanderveken M, O’Donnell MJ (2014) The heterodimeric glycoprotein hormone, GPA2/GPB5, regulates ion transport across the hindgut of the adult mosquito, Aedes aegypti. PLoS ONE 9:e86386CrossRefPubMedPubMedCentralGoogle Scholar
  25. Percy R, Leatherland JF, Beamish FW (1975) Structure and ultrastructure of the pituitary gland in the sea lamprey, Petromyzon marinus at different stages in its life cycle. Cell Tissue Res 157:141–164CrossRefPubMedGoogle Scholar
  26. Root AR, Nucci NV, Sanford JD, Rubin BS, Trudeau VL, Sower SA (2005) In situ characterization of gonadotropin- releasing hormone-I, -III, and glutamic acid decarboxylase expression in the brain of the sea lamprey, Petromyzon marinus. Brain Behav Evol 65:60–70CrossRefPubMedGoogle Scholar
  27. Rubin BS, Lee CE, Ohtomo M, King JC (1997) Luteinizing hormone-releasing hormone gene expression differs in young and middle-aged females on the day of a steroid-induced LH surge. Brain Res 770:267–276CrossRefPubMedGoogle Scholar
  28. Sellami A, Agricola HJ, Veenstra JA (2011) Neuroendocrine cells in Drosophila melanogaster producing GPA2/GPB5, a hormone with homology to LH, FSH and TSH. Gen Comp Endocrinol 170:582–588CrossRefPubMedGoogle Scholar
  29. Slidders W (1961) The OFG and BrAB-OFG methods for staining the adenohypophysis. J Pathol Bacteriol 82:532–534CrossRefPubMedGoogle Scholar
  30. Smith AI, Funder JW (1988) Proopiomelanocortin processing in the pituitary, central nervous system, and peripheral tissues. Endocr Rev 9:159–179CrossRefPubMedGoogle Scholar
  31. Sower SA (2003) The endocrinology of reproduction in lampreys and applications for male lamprey sterilization. J Great Lakes Res 29:50–65CrossRefGoogle Scholar
  32. Sower SA, Baron MP (2011) The interrelationship of estrogen receptor and GnRH in a Basal vertebrate, the sea lamprey. Front Endocrinol (Lausanne) 2:58Google Scholar
  33. Sower SA, Decatur WA, Hausken KN, Marquis TJ, Barton SL, Gargan J, Freamat M, Wilmot M, Hollander L, Hall JA, Nozaki M, Shpilman M, Levavi-Sivan B (2015) Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate. Endocrinology 156:3026–3037CrossRefPubMedGoogle Scholar
  34. Sower SA, Freamat M, Kavanaugh SI (2009) The origins of the vertebrate hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-thyroid (HPT) endocrine systems: new insights from lampreys. Gen Comp Endocrinol 161:20–29CrossRefPubMedGoogle Scholar
  35. Sower SA, King JA, Millar RP, Sherwood NM, Marshak DR (1987) Comparative biological properties of lamprey gonadotropin-releasing hormone in vertebrates. Endocrinology 120:773–779CrossRefPubMedGoogle Scholar
  36. Sower SA, Moriyama S, Kasahara M, Takahashi A, Nozaki M, Uchida K, Dahlstrom JM, Kawauchi H (2006) Identification of sea lamprey GTHbeta-like cDNA and its evolutionary implications. Gen Comp Endocrinol 148:22–32CrossRefPubMedGoogle Scholar
  37. Swanson P, Dickey JT, Campbell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:53–59CrossRefGoogle Scholar
  38. Szkudlinski MW, Fremont V, Ronin C, Weintraub BD (2002) Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationships. Physiol Rev 82:473–502CrossRefPubMedGoogle Scholar
  39. Takahashi A, Amemiya Y, Nozaki M, Sower SA, Joss J, Gorbman A, Kawauchi H (1995a) Isolation and characterization of melanotropins from lamprey pituitary glands. Int J Pept Protein Res 46:197–204CrossRefPubMedGoogle Scholar
  40. Takahashi A, Amemiya Y, Sarashi M, Sower SA, Kawauchi H (1995b) Melanotropin and corticotropin are encoded on two distinct genes in the lamprey, the earliest evolved extant vertebrate. Biochem Biophys Res Commun 213:490–498CrossRefPubMedGoogle Scholar
  41. Takahashi A, Yasuda A, Sower SA, Kawauchi H (2006) Posttranslational processing of proopiomelanocortin family molecules in sea lamprey based on mass spectrometric and chemical analyses. Gen Comp Endocrinol 148:79–84CrossRefPubMedGoogle Scholar
  42. Themmen APN, Huhtaniemi IT (2000) Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr Rev 21:551–583CrossRefPubMedGoogle Scholar
  43. Tsuneki K, Gorbman A (1975a) Ultrastructure of pars nervosa and pars intermedia of the Lamprey, Lampetra tridentata. Cell Tissue Res 157:165–184CrossRefPubMedGoogle Scholar
  44. Tsuneki K, Gorbman A (1975b) Ultrastructure of the anterior neurohypophysis and the pars distalis of the lamprey, Lampetra tridentata. Gen Comp Endocrinol 25:487–508CrossRefPubMedGoogle Scholar
  45. Uchida K, Moriyama S, Chiba H, Shimotani T, Honda K, Miki M, Takahashi A, Sower SA, Nozaki M (2010) Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish. Proc Natl Acad Sci U S A 107:15832–15837CrossRefPubMedPubMedCentralGoogle Scholar
  46. Walker CW, Harrington LM, Lesser MP, Fagerberg WR (2005) Nutritive phagocyte incubation chambers provide a structural and nutritive microenvironment for germ cells of Strongylocentrotus droebachiensis, the green sea urchin. Biol Bull 209:31–48CrossRefPubMedGoogle Scholar
  47. Wang F, Flanagan J, Su N, Wang LC, Bui S, Nielson A, Wu X, Vo HT, Ma XJ, Luo Y (2012) RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 14:22–29CrossRefPubMedPubMedCentralGoogle Scholar
  48. Weibel ER (1979) Stereological methods. Academic, LondonGoogle Scholar
  49. Wilcox JN (1993) Fundamental principles of in situ hybridization. J Histochem Cytochem 41:1725–1733CrossRefPubMedGoogle Scholar
  50. Yoshimura F (1984) A new concept of anterior pituitary cell classification in the rat based on both cell differentiation and the secretory cycle. In: Yoshimura R, Gorbman A (eds) First international symposium on the pituitary gland. Elsevier, Tokyo, pp 59–69Google Scholar
  51. Youson JH, Heinig JA, Khanam SF, Sower SA, Kawauchi H, Keeley FW (2006) Patterns of proopiomelanotropin and proopiocortin gene expression and of immunohistochemistry for gonadotropin-releasing hormones (lGnRH-I and III) during the life cycle of a nonparasitic lamprey: relationship to this adult life history type. Gen Comp Endocrinol 148:54–71CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Timothy J. Marquis
    • 1
    • 2
  • Masumi Nozaki
    • 3
  • Wayne Fagerberg
    • 2
  • Stacia A. Sower
    • 1
    • 2
  1. 1.Center for Molecular and Comparative EndocrinologyUniversity of New HampshireDurhamUSA
  2. 2.Department of Molecular, Cellular and Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.Sado Marine Biological StationNiigata UniversitySadoJapan

Personalised recommendations