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Apparent Involvement of a β1 Type Integrin in Coral Fertilization

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Abstract

Integrins are involved in a wide variety of cell adhesion processes, and have roles in gamete binding and fusion in mammals. Integrins have been also discovered in the scleractinian coral Acropora millepora (Cnidaria: Anthozoa). As a first step toward understanding the molecular basis of fertilization in corals, we examined the effect of polyclonal antisera raised against recombinant coral integrins on gamete interactions in A. millepora. Antiserum raised against integrin βcn1 dramatically decreased the binding of Acropora sperm to eggs and significantly decreased fertilization rates relative to preimmune serum and seawater controls. However, the antiserum against AmIntegrin α1 did not affect significantly either sperm–egg binding or fertilization. One possible explanation for this is that AmIntegrin α1 may preferentially mediate interactions with RGD-containing ligands, whereas mammalian α6 integrin (which is most directly implicated in gamete interactions) preferentially interacts with laminin-related ligands. Our results suggest that β1 type integrins are involved in the fertilization process in Acropora and that some functions of these molecules may have been conserved between corals and mammals.

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References

  • Almeida EAC, Huovila APJ, Sutherland AE, Stephens LE, Calarco PG, Shaw LM, Mercurio AM, Sonnenberg A, Primakoff P, Myles DG, White JM (1995) Mouse egg integrin α6β1 functions as a sperm receptor. Cell 81, 1095–1104

    Article  PubMed  CAS  Google Scholar 

  • Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawning of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90, 379–394

    Article  Google Scholar 

  • Ball EE, Hayward DC, Saint R, Miller DJ (2004) A simple plan—Cnidarians and the origins of developmental mechanisms. Nat Rev Genet 5, 567–577

    Article  PubMed  CAS  Google Scholar 

  • Bigler D, Takahashi Y, Chen MS, Almeida EAC, Osbourne L, White JM (2000) Sequence-specific interaction between the disintegrin domain of mouse ADAM2 (fertilin β) and murine eggs. J Biol Chem 275, 11576–11584

    Article  PubMed  CAS  Google Scholar 

  • Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci 58, 1189–1205

    Article  PubMed  CAS  Google Scholar 

  • Brower DL, Brower SM, Hayward DC, Ball EE (1997) Molecular evolution of integrins: genes encoding integrin β subunits from a coral and a sponge. Proc Natl Acad Sci USA 94, 9182–9187

    Article  PubMed  CAS  Google Scholar 

  • Eto K, Huet C, Tarui T, Kupriyanov S, Liu HZ, Puzon-McLaughlin W, Zhang XP, Sheppard D, Engvall E, Takada Y (2002) Functional classification of ADAMs based on a conserved motif for binding to integrin α9β1. J Biol Chem 277, 17804–17810

    Article  PubMed  CAS  Google Scholar 

  • Evans JP (2002) The molecular basis of sperm–oocyte membrane interactions during mammalian fertilization. Hum Reprod 8, 297–311

    Article  CAS  Google Scholar 

  • Evans JP, Kopf GS, Schultz RM (1997a) Characterization of the binding of fusion mouse sperm fertilin β subunit to mouse eggs: evidence for adhesive activity via an egg β1 integrin-mediated interaction. Dev Biol 187, 79–93

    Article  PubMed  CAS  Google Scholar 

  • Evans JP, Schultz RM, Kopf GS (1997b) Characterization of the binding of fusion mouse sperm fertilin α subunit to mouse eggs: evidence for function as a cell adhesion molecule in sperm-egg binding. Dev Biol 187, 94–106

    Article  PubMed  CAS  Google Scholar 

  • Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223, 1186–1189

    Article  PubMed  CAS  Google Scholar 

  • Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, Kudo K, Omori M (1993) Patterns of coral spawning at Akajima Island, Okinawa, Japan. Mar Ecol Prog Ser 101, 253–262

    Article  Google Scholar 

  • He ZY, Brakebusch C, Fassler R, Kreidberg JA, Primakoff P, Myles DG (2003) None of the integrins known to be present on the mouse egg or to be ADAM receptors are essential for sperm–egg binding and fusion. Dev Biol 254, 226–237

    Article  PubMed  CAS  Google Scholar 

  • Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687

    Article  PubMed  CAS  Google Scholar 

  • Kaji K, Kudo A (2004) The mechanism of sperm–oocyte fusion in mammals. Reproduction 127, 423–429

    Article  PubMed  CAS  Google Scholar 

  • Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 16, 2190–2195

    Article  CAS  Google Scholar 

  • Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, Holstein TW (2004) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156–160

    Article  CAS  Google Scholar 

  • Le Naour F, Rubinstein E, Jasmin C, Prenanrt M, Boucheix C (2000) Severely reduced female fertility in CD9-deficient mice. Science 287, 319–321

    Article  PubMed  Google Scholar 

  • Márquez LM, van Oppen MJH, Willis BL, Miller DJ (2002a) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and A. cytherea are genetically distinct. Proc R Soc Lond B Biol Sci 269, 1289–1294

    Article  Google Scholar 

  • Márquez LM, van Oppen MJH, Willis BL, Reyes A, Miller DJ (2002b) The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Mol Ecol 11, 1339–1349

    Article  PubMed  Google Scholar 

  • Miller BJ, Georges-Labouesse E, Primakoff P, Myles DG (2000) Normal fertilization occurs with eggs lacking the integrin α6β1 and is CD9-dependent. J Cell Biol 149, 1289–1295

    Article  PubMed  CAS  Google Scholar 

  • Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryo F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Medaka E (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287, 321–324

    Article  PubMed  CAS  Google Scholar 

  • Omori M, Fukami H, Kobinata H, Hatta M (2001) Significant drop of fertilization of Acropora corals in 1999: an after-effect of heavy coral bleaching? Limnol Oceanogr 46, 704–706

    Article  Google Scholar 

  • Reber-Muller S, Studer R, Muller P, Yanze N, Schmid V (2001) Integrin and talin in the jellyfish Podocoryne carnea. Cell Biol Int 25, 753–769

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1992) Molecular Cloning: A Laboratory Manual, 2nd ed (Plainview, NY: Cold Spring Harbor Laboratory Press)

    Google Scholar 

  • Takahashi Y, Bigler D, Ito Y, White JM (2001) Sequence-specific interaction between the disintegrin domain of mouse ADAM 3 and murine eggs: role of β1 integrin-associated proteins CD9, CD81, and CD98. Mol Biol Cell 12, 809–820

    PubMed  CAS  Google Scholar 

  • Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21, 633–639

    Article  PubMed  CAS  Google Scholar 

  • Veron JEN (2000) Corals of the World. (Townsville, Queensland, Australia: Australian Institute of Marine Science).

    Google Scholar 

  • Wallace CC (1999) Staghorn corals of the world: a revision of the genus Acropora. (Collingwood, Australia: CSIRO Publishing).

    Google Scholar 

  • Whittaker CA, DeSimone DW (1993) Integrin alpha subunit mRNAs are differentially expressed in early Xenopus embryos. Development 117, 1239–1249

    PubMed  CAS  Google Scholar 

  • Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16 (Suppl), s53–s65

    Article  Google Scholar 

  • Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37, 489–517

    Article  Google Scholar 

  • Ziyyat A, Rubinstein E, Monier-Gavelle F, Barraud V, Kulski O, Prenant M, Boucheix C, Bomsel M, Wolf JP (2006) CD9 controls the formation of clusters that contain tetraspanins and the integrin α6β1, which are involved in human and mouse gamete fusion. J Cell Sci 119, 416–424

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the support of the Australian Research Council (ARC) both directly to D.J.M. (Grants A00105431, DP0209460, and DP0344483) and via the Centre for the Molecular Genetics of Development and the Centre of Excellence for Coral Reef Studies. A.I. and C.S. acknowledge receipt of scholarships from the Okinawa International Exchange & Human Resources Development Foundation. L.M.M. acknowledges the receipt of a scholarship from the Venezuelan Fund for Scientific and Technologic Research (FONACIT).

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Authors and Affiliations

  1. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Australia, Townsville, Queensland, 4811, Australia

    Akira Iguchi, Luis M. Márquez, Brent Knack, Chuya Shinzato,  Madeleine J. H. van Oppen, Bette L. Willis, Kate Hardie, Julian Catmull &  David J. Miller

  2. Comparative Genomics Centre, James Cook University, Australia, Townsville, Queensland, 4811, Australia

    Akira Iguchi, Luis M. Márquez, Brent Knack, Chuya Shinzato, Kate Hardie, Julian Catmull &  David J. Miller

  3. Australian Institute of Marine Science, PMB No 3, Queensland, 4810, Australia

    Madeleine J. H. van Oppen

  4. Marine Biology and Aquaculture, James Cook University, Townsville, Queensland, 4811, Australia

    Bette L. Willis

  5. Centro de Biotecnologia, Instituto de Estudios Avanzados IDEA Valle de Sartenejas, Baruta. Edo. Miranda, Caracas, 1015-A, Venezuela

    Luis M. Márquez

Authors
  1. Akira Iguchi
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  2. Luis M. Márquez
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  3. Brent Knack
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  4. Chuya Shinzato
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  5. Madeleine J. H. van Oppen
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  6. Bette L. Willis
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  7. Kate Hardie
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  8. Julian Catmull
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  9. David J. Miller
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Corresponding author

Correspondence to David J. Miller.

Additional information

A. Iguchi and L. M. Márquez contributed equally to this work.

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Iguchi, A., Márquez, L.M., Knack, B. et al. Apparent Involvement of a β1 Type Integrin in Coral Fertilization. Mar Biotechnol 9, 760–765 (2007). https://doi.org/10.1007/s10126-007-9026-0

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  • DOI: https://doi.org/10.1007/s10126-007-9026-0

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