Mammalian Genome

, Volume 17, Issue 8, pp 858–877 | Cite as

The rat prolactin gene family locus: species-specific gene family expansion

  • S.M. Khorshed Alam
  • Rupasri Ain
  • Toshihiro Konno
  • Jennifer K. Ho-Chen
  • Michael J. Soares


In the rat there is a large family of paralogous genes related to prolactin (PRL). Members of the PRL family are expressed in cell- and temporal-specific patterns in the anterior pituitary, uterus, and placenta. An overriding feature of the PRL family is its association with pregnancy. In this investigation, we used information derived from the public rat genome database as a tool for identifying new members of the rat PRL family. The entire rat PRL gene family locus spans approximately 1.7 megabases (Mb) on Chromosome 17. Genes possessed either 5- or 6-exon organization patterns. We provide information on three newly identified genes orthologous to previously identified members of the mouse PRL gene family [placental lactogen-Iα (PL-Iα), PL-Iβ, and proliferin (PLF)] and a new member of the PRL family, termed PRL-like protein-P (PLP-P). Information is also presented on the existence of multiple PLP-M transcripts, which are generated by alternative splicing. Expansion of the PRL family has occurred independently in rodents versus the cow and does not exist in the human and dog. Elucidation of the rat PRL gene family locus provides tools for studying the genetics and biology of the rat PRL family and new insights into species-specific gene family expansion.


Trophoblast Cell Junctional Zone Trophoblast Giant Cell Exon Versus Chorioallantoic Placenta 
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  1. Ain R, Canham LN, Soares MJ (2003) Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol 260; 176–190PubMedCrossRefGoogle Scholar
  2. Ain R, Dai G, Dunmore JH, Godwin AR, Soares MJ (2004) A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc Natl Acad Sci USA 101: 16543–16548PubMedCrossRefGoogle Scholar
  3. Ain R, Konno T, Canham LN, Soares MJ (2006) Phenotypic analysis of the placenta in the rat. In Placenta and Trophoblast: Methods and Protocols, Vol. I, Soares MJ, Hunt JS (eds.) (Totowa, NJ: Humana Press), pp 295–313Google Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410PubMedCrossRefGoogle Scholar
  5. Astwood EB, Greep RO (1938) A corpus luteum stimulating substance in the rat placenta. Proc Soc Exp Biol Med 38: 713–716Google Scholar
  6. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA (1998) Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19: 225–268PubMedCrossRefGoogle Scholar
  7. Braissant O, Wahli W (1998) A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1: 10–16Google Scholar
  8. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156–159PubMedCrossRefGoogle Scholar
  9. Clapp C, Sears PS, Russell DH, Richards J, Levay-Young BK, et al. (1988) Biological and immunological characterization of cleaved and 16K forms of rat prolactin. Endocrinology 122: 2892PubMedGoogle Scholar
  10. Cohick CB, Dai G, Xu L, Deb S, Kamei T, et al. (1996) Placental lactogen-I variant utilizes the prolactin receptor signaling pathway. Mol Cell Endocrinol 116: 49–58PubMedCrossRefGoogle Scholar
  11. Colosi P, Ogren L, Thordarson G, Talamantes F (1987a) Purification and partial characterization of two prolactin-like glycoprotein hormone complexes from the midpregnant mouse conceptus. Endocrinology 120: 2500–2511Google Scholar
  12. Colosi P, Talamantes F, Linzer DIH (1987b) Molecular cloning and expression of mouse placental lactogen I complementary deoxyribonucleic acid. Mol Endocrinol 1: 767–776Google Scholar
  13. Colosi P, Ogren L, Southard JN, Thordarson G, Linzer DI, et al. (1988) Biological, immunological, and binding properties of recombinant mouse placental lactogen-I. Endocrinology 123: 2662–2667PubMedGoogle Scholar
  14. Cooke NE, Liebhaber SA (1995) Molecular biology of the growth hormone-prolactin gene system. Vitam Horm 50: 385–459PubMedCrossRefGoogle Scholar
  15. Cooke NE, Coit D, Weiner RI, Baxter JD, Martial JA (1980) Structure of cloned DNA complementary to rat prolactin messenger RNA. J Biol Chem 255: 6502–6510PubMedGoogle Scholar
  16. Corbacho AM, Martinez de la Escalera G, Clapp C (2002) Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 173: 219–238PubMedCrossRefGoogle Scholar
  17. Dai G, Imagawa W, Liu B, Szpirer C, Levan G, et al. (1996a) Rcho-1 trophoblast cell placental lactogens: complementary deoxyribonucleic acids, heterologous expression, and biological activities. Endocrinology 137: 5020–5027CrossRefGoogle Scholar
  18. Dai G, Liu B, Szpirer C, Levan G, Kwok SCM, et al. (1996b) Prolactin-like protein-C variant: complementary deoxyribonucleic acid, unique six exon gene structure, and trophoblast cell-specific expression. Endocrinology 137: 5009–5019CrossRefGoogle Scholar
  19. Dai G, Wang D, Liu B, Kasik JW, Müller H, et al. (2000) Three novel paralogs of the rodent prolactin gene family. J Endocrinol 166: 63–75PubMedCrossRefGoogle Scholar
  20. Dai G, Lu L, Tang S, Peal MJ, Soares MJ (2002) Prolactin family miniarray: a tool for evaluating uteroplacental-trophoblast endocrine cell phenotypes. Reproduction 124: 755–765PubMedCrossRefGoogle Scholar
  21. Deb S, Faria TN, Roby KF, Larsen D, Kwok SC, et al. (1991a) Identification and characterization of a new member of the prolactin family, placental lactogen-I variant. J Biol Chem 266: 1605–1610Google Scholar
  22. Deb S, Roby KF, Faria TN, Larsen D, Soares MJ (1991b) Identification and immunochemical characterization of a major placental secretory protein related to the prolactin-growth hormone family, prolactin-like protein-C. Endocrinology 128: 3066–3072Google Scholar
  23. Deb S, Roby KF, Faria TN, Szpirer C, Levan G, et al. (1991c) Molecular cloning and characterization of prolactin-like protein C complementary deoxyribonucleic acid. J Biol Chem 266: 23027–23032Google Scholar
  24. Deussing J, Kouadio M, Rehman S, Werber I, Schwinde A, et al. (2002) Identification and characterization of a dense cluster of placenta-specific cysteines peptidase genes and related genes on mouse chromosome 13. Genomics 79: 225–240PubMedCrossRefGoogle Scholar
  25. Dorshkind K, Horseman ND (2001) Anterior pituitary hormones, stress, and immune system homeostasis. BioEssays 23: 288–294PubMedCrossRefGoogle Scholar
  26. Duckworth ML, Kirk KL, Friesen HG (1986a) Isolation and identification of a cDNA clone of rat placental lactogen II. J Biol Chem 261: 10871–10878Google Scholar
  27. Duckworth ML, Peden LM, Friesen HG (1986b) Isolation of a novel prolactin-like cDNA clone from developing rat placenta. J Biol Chem 261: 10879–10884Google Scholar
  28. Duckworth ML, Peden LM, Friesen HG (1988) A third prolactin-like protein expressed by the developing rat placenta: complementary deoxyribonucleic acid sequence and partial structure of the gene. Mol Endocrinol 2: 912–920PubMedGoogle Scholar
  29. Faria TN, Soares MJ (1991) Trophoblast cell differentiation: establishment, characterization, and modulation of a rat trophoblast cell line expressing members of the placental prolactin family. Endocrinology 129: 2895–2906PubMedGoogle Scholar
  30. Faria TN, Deb S, Kwok SCM, Talamantes F, Soares MJ (1990) Ontogeny of placental lactogen-I and placental lactogen-II expression in the developing rat placenta. Dev Biol 141: 279–291PubMedCrossRefGoogle Scholar
  31. Faria TN, Ogren L, Talamantes F, Linzer DI, Soares MJ (1991) Localization of placental lactogen-I in trophoblast giant cells of the mouse placenta. Biol Reprod 44: 327–331PubMedCrossRefGoogle Scholar
  32. Fassett JT, Nilsen-Hamilton M (2001) Mrp3, a mitogen-regulated protein/proliferin gene expressed in wound healing and in hair follicles. Endocrinology 142: 2129–2137PubMedCrossRefGoogle Scholar
  33. Fassett JT, Hamilton RT, Nilsen-Hamilton M (2000) Mrp4, a new mitogen-regulated protein/proliferin gene; unique in this gene family for its expression in the adult mouse tail and ear. Endocrinology 141: 1863–1871PubMedCrossRefGoogle Scholar
  34. Forsyth IA, Wallis M (2002) Growth hormone and prolactin. Molecular and functional evolution. J Mammary Gland Biol Neoplasia 7: 291–312PubMedCrossRefGoogle Scholar
  35. Francino MP (2005) An adaptive radiation model for the origin of new gene functions. Nat Genet 37: 573–577PubMedCrossRefGoogle Scholar
  36. Goffin V, Binart N, Touraine P, Kelly PA (2002) Prolactin: the new biology of an old hormone. Annu Rev Physiol 64: 47–67PubMedCrossRefGoogle Scholar
  37. Gubbins EJ, Maurer RA, Hartley JL, Donelson JE (1979) Construction and analysis of recombinant DNAs containing a structural gene for rat prolactin. Nucleic Acids Res 6: 915–930PubMedGoogle Scholar
  38. Hiraoka Y, Ogawa M, Sakai Y, Takeuchi Y, Komatsu N, et al. (1999) PLP-I: a novel prolactin-like gene in rodents. Biochem Biophys Acta 1447: 291–297PubMedGoogle Scholar
  39. Hirosawa M, Miura R, Min KS, Hattori N, Shiota K, et al. (1994) A cDNA encoding a new member of the rat placental lactogen family, PL-I mosaic (PL-Im). Endocr J 41: 387–397PubMedGoogle Scholar
  40. Hughes AL, Green JA, Piontkivska H, Roberts RM (2003) Aspartic proteinase phylogeny and the origin of pregnancy-associated glycoproteins. Mol Biol Evol 20: 1940–1945PubMedCrossRefGoogle Scholar
  41. Hwang IT, Lee YH, Moon BC, Ahn KY, Lee SW, et al. (2000) Identification and characterization of a new member of the placental prolactin-like protein-C (PLP-C) subfamily, PLP-Cβ. Endocrinology 141: 3343–3352PubMedCrossRefGoogle Scholar
  42. Ishibashi K, Imai M (1999) Identification of four new members of the rat prolactin/growth hormone gene family. Biochem Biophys Res Commun 262: 575–578PubMedCrossRefGoogle Scholar
  43. Iwatsuki K, Shinozaki M, Hattori N, Hirasawa K, Itagaki S, et al. (1996) Molecular cloning and characterization of a new member of the rat placental prolactin (PRL) family, PRL-like protein D (PLP-D). Endocrinology 137: 3849–3855PubMedCrossRefGoogle Scholar
  44. Iwatsuki K, Oda M, Sun W, Tanaka S, Ogawa T, et al. (1998) Molecular cloning and characterization of a new member of the rat placental prolactin (PRL) family, PRL-like protein H. Endocrinology 139: 4976–4983PubMedCrossRefGoogle Scholar
  45. Jackson D, Volpert OV, Bouck N, Linzer DIH (1994) Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein. Science 266: 1581–1584PubMedGoogle Scholar
  46. Kelly PA, Shiu RP, Robertson MC, Friesen HG (1975) Characterization of rat chorionic mammotropin. Endocrinology 96: 1187–1195PubMedGoogle Scholar
  47. Kopelman NM, Lancet D, Yanai I (2005) Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet 37: 588–589PubMedCrossRefGoogle Scholar
  48. Lee SJ, Talamantes F, Wilder E, Linzer DIH, Nathans D (1988) Trophoblastic giant cells of the mouse placenta as the site of proliferin synthesis. Endocrinology 122: 1761–1768PubMedGoogle Scholar
  49. Lewis UJ (1984) Variants of growth hormone and prolactin and their posttranslational modifications. Annu Rev Physiol 46: 33–42PubMedCrossRefGoogle Scholar
  50. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803–819PubMedCrossRefGoogle Scholar
  51. Linzer DIH, Lee SJ, Ogren L, Talamantes F, Nathans D (1985) Identification of proliferin mRNA and protein in mouse placenta. Proc Natl Acad Sci USA 82: 4356–4359PubMedCrossRefGoogle Scholar
  52. MacLean JA, Chakrabarty A, Xie S, Bixby JA, Roberts RM, et al. (2003) Family of Kunitz proteins from trophoblast: expression of Kunitz domain proteins in cattle and sheep. Mol Reprod Dev 65: 30–40PubMedCrossRefGoogle Scholar
  53. MacLean JA, Chen MA, Wayne CM, Bruce SR, Rao M, et al. (2005) Rhox: a new homeobox gene cluster. Cell 120: 369–382PubMedCrossRefGoogle Scholar
  54. MacLean JA, Lorenzetti D, Hu Z, Salerno WJ, Miller J, et al. (2006) Rhox homeobox gene cluster: recent duplication of three family members. Genesis 44: 122–129PubMedCrossRefGoogle Scholar
  55. Mallon A-M, Wilming L, Weekes J, Gilbert JGR, Ashurst J, et al. (2004) Organziation and evolution of a gene-rich region of the mouse genome: a 12.7 Mb region deleted in the Del(13)Svea36H mouse. Genome Res 14: 1888–1901PubMedCrossRefGoogle Scholar
  56. Markoff E, Sigel MB, Lacour N, Seavey BK, Friesen HG, et al. (1988) Glycosylation selectively alters the biological activity of prolactin. Endocrinology 123: 1303–136PubMedGoogle Scholar
  57. Mason RW, Stabley DL, Picerno GN, Frenck J, Xing S, et al. (2002) Evolution of placental proteases. Biol Chem 383: 1113–1118PubMedCrossRefGoogle Scholar
  58. Maston GA, Ruvolo M (2002) Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection. Mol Biol Evol 19: 320–335PubMedGoogle Scholar
  59. McLellan AS, Fischer B, Dveksler G, Hori T, Wyne F, et al. (2005a) Structure and evolution of the mouse pregnancy-specific glycoprotein (Psg) gene locus. BMC Genomics 6: 4CrossRefGoogle Scholar
  60. McLellan AS, Zimmerman W, Moore T (2005b) Conservation of pregnancy-specific glycoprotein (PSG) N domains following independent expansions of the gene families in rodents and primates. BMC Evolutionary Biol 5: 39CrossRefGoogle Scholar
  61. Mouse Genome Sequencing Consortium (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520–562CrossRefGoogle Scholar
  62. Niall HD, Hogan ML, Sauer R, Rosenblum IY, Greenwood FC (1971) Sequences of pituitary and placental lactogenic and growth hormones: evolution from a primordial peptide by gene duplication. Proc Natl Acad Sci USA 68: 866–870PubMedCrossRefGoogle Scholar
  63. Nicoll CS (1980) Ontogeny and evolution of prolactin’s functions. Fed Proc 39: 2563–2566PubMedGoogle Scholar
  64. Nicoll CS, Bern HA (1972) On the actions of prolactin among the vertebrates: is there a common denominator? In Lactogenic Hormones, Wolstenholme GEW, Knight J (eds.) (London: Churchill Livingstone), pp 299–337Google Scholar
  65. Nicoll CS, Mayer GL, Russell SM (1986) Structural features of prolactins and growth hormones that can be related to their biological properties. Endocr Rev 7: 169–203PubMedGoogle Scholar
  66. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1–66PubMedCrossRefGoogle Scholar
  67. Oetting WS, Tuazon PT, Traugh JA, Walker AM (1988) Phosphorylation of prolactin. J Biol Chem 261: 1649–1652Google Scholar
  68. Ozturk A, Fresnoza A, Savoie A, Duckworth HW, Duckworth ML (2003) Defining regulatory regions in the rat prolactin gene family locus using a large P1 genomic clone. Endocrinology 144: 4742–4754PubMedCrossRefGoogle Scholar
  69. Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358PubMedGoogle Scholar
  70. Pencharz RL, Long JA (1931) The effect of hypophysectomy on gestation in the rat. Science 74, 206PubMedGoogle Scholar
  71. Rat Genome Sequencing Project Consortium (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428: 493–521CrossRefGoogle Scholar
  72. Roberts RM, Ezashi T, Rosenfeld CS, Ealy AD, Kubisch HM (2003) Evolution of interferon tau genes and their promoters, and maternal-trophoblast interactions in control of their expression. Reprod Suppl 61: 239–251PubMedGoogle Scholar
  73. Robertson MC, Friesen HG (1975) The purification and characterization of rat placental lactogen. Endocrinology 97: 621–629Google Scholar
  74. Robertson MC, Friesen HG (1981) Two forms of rat placental lactogen revealed by radioimmunoassay. Endocrinology 108: 2388–2390PubMedCrossRefGoogle Scholar
  75. Robertson MC, Croze F, Schroedter IC, Friesen HG (1990) Molecular cloning and expression of rat placental lactogen-I complementary deoxyribonucleic acid. Endocrinology 127: 702–710PubMedGoogle Scholar
  76. Robertson MC, Schroedter IC, Friesen HG (1991) Molecular cloning and expression of rat placental lactogen-Iv, a variant of rPL-I present in late pregnant rat placenta. Endocrinology 129: 2746–2756PubMedCrossRefGoogle Scholar
  77. Robertson MC, Cosby H, Shiu RP (1996) Rat placental lactogen-I variant (rPL-Iv), product of an unique gene, is biologically different from rPL-I. Endocrinology 137: 5242–5249PubMedCrossRefGoogle Scholar
  78. Roby KF, Deb S, Gibori G, Szpirer C, Levan G, et al. (1993) Decidual prolactin-related protein. Identification, molecular cloning, and characterization. J Biol Chem 268: 3136–3142PubMedGoogle Scholar
  79. Sahgal N, Knipp GT, Liu B, Chapman BM, Dai G, et al. (2000) Identification of two new nonclassical members of the rat prolactin family. J Mol Endocrinol 24: 95–108PubMedCrossRefGoogle Scholar
  80. Sahgal N, Canham LN, Canham B, Soares MJ (2006) Rcho-1 trophoblast cells: a model for studying trophoblast differentiation. In Placenta and Trophoblast: Methods and Protocols, Vol. 1, Soares MJ, Hunt JS (eds.) (Totowa, NJ: Humana Press), pp 159–178Google Scholar
  81. Schuler LA, Kessler MA (1992) Bovine placental prolactin-related hormones. Trends Endocrinol Metabol 3: 334–338CrossRefGoogle Scholar
  82. Sigmund CD, Gross KW (1991) Structure, expression, and regulation of the murine renin genes. Hypertension 18, 446–457PubMedGoogle Scholar
  83. Sinha YN (1995) Structural variants of prolactin: occurrence and physiological significance. Endocr Rev 16: 354–369PubMedCrossRefGoogle Scholar
  84. Soares MJ (2004) The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol 2: 51PubMedCrossRefGoogle Scholar
  85. Soares MJ, Julian JA, Glasser SR (1985) Trophoblast giant cell release of placental lactogens: temporal and regional characteristics. Dev Biol 107: 520–526PubMedCrossRefGoogle Scholar
  86. Sol-Church K, Picerno GN, Stabley DL, Frenck J, Xing S, et al. (2002) Evolution of placentally expressed cathepsins. Biochem Biophys Res Commun 293: 23–29PubMedCrossRefGoogle Scholar
  87. Tanaka TS, Jaradat SA, Lim MK, Kargul GJ, Wang X, et al. (2000) Genome-wide expression profiling of mid-gestation placenta and embryo using 15,000 mouse developmental cDNA microarray. Proc Natl Acad Sci USA 97: 9127–9132PubMedCrossRefGoogle Scholar
  88. Telgmann R, Gellersen B (1998) Marker genes of decidualization: activation of the decidual prolactin gene. Hum Reprod Update 4: 472–479PubMedCrossRefGoogle Scholar
  89. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680PubMedGoogle Scholar
  90. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882PubMedCrossRefGoogle Scholar
  91. Toft DJ, Linzer DIH (1999) Prolactin (PRL)-like protein J, a novel member of the PRL/growth hormone family, is exclusively expressed in maternal decidua. Endocrinology 140: 5095–5101PubMedCrossRefGoogle Scholar
  92. Toft DJ, Linzer DIH (2000) Identification of three prolactin-related hormones as markers of invasive trophoblasts in the rat. Biol Reprod 63: 519–525PubMedCrossRefGoogle Scholar
  93. Toft DJ, Rosenberg SB, Bergers G, Volpert O, Linzer DIH (2001) Reactivation of proliferin gene expression is associated with increased angiogenesis in a cell culture model of fibrosarcoma tumor progression. Proc Natl Acad Sci USA 98: 13055–13059PubMedCrossRefGoogle Scholar
  94. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, et al. (2001) The sequence of the human genome. Science 291: 1304–1351PubMedCrossRefGoogle Scholar
  95. Vrana PB, Matteson PG, Schmidt JV, Ingram RS, Joyce A, et al. (2001) Genomic imprinting of a placental lactogen gene in Peromyscus. Dev Genes Evol 211: 523–532PubMedCrossRefGoogle Scholar
  96. Wallis M (1992) The expanding growth hormone/prolactin family. J Mol Endocrinol 9: 185–188PubMedCrossRefGoogle Scholar
  97. Wicks JR, Brooks CL (1995) Biological activity of phosphorylated and dephosphorylated bovine prolactin. Mol Cell Endocrinol 112: 223–229PubMedCrossRefGoogle Scholar
  98. Wiemers DO, Ain R, Ohboshi S, Soares MJ (2003a) Migratory trophoblast cells express a newly identified member of the prolactin gene family. J Endocrinol 179: 335–346CrossRefGoogle Scholar
  99. Wiemers DO, Shao L-J, Ain R, Dai G, Soares MJ (2003b) The mouse prolactin gene family locus. Endocrinology 144: 313–325CrossRefGoogle Scholar
  100. Wilder EL, Linzer DIH (1986) Expression of multiple proliferin genes in mouse cells. Mol Cell Biol 6: 3283–3286PubMedGoogle Scholar
  101. Xie S, Green J, Bixby JB, Szafranska B, De Martini JC, et al. (1997) The diversity and evolutionary relationships of the pregnancy-associated glycoproteins, an aspartic proteinase subfamily consisting of many trophoblast-expressed genes. Proc Natl Acad Sci USA 94: 12809–12816PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • S.M. Khorshed Alam
    • 1
  • Rupasri Ain
    • 1
  • Toshihiro Konno
    • 1
  • Jennifer K. Ho-Chen
    • 1
  • Michael J. Soares
    • 1
  1. 1.Institute of Maternal-Fetal Biology and the Division of Cancer & Developmental Biology, Departments of Pathology and Laboratory Medicine and Obstetrics and GynecologyUniversity of Kansas Medical CenterKansas CityUSA

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