Farewell to Professor David Yaffe – A Pillar of the Myogenesis Field


Published: 18 August 2020
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Authors

  • Zipora Yablonka-Reuveni Department of Biological Structure, University of Washington School of Medicine, Seattle, WA, United States.
  • Frank Stockdale Stanford University School of Medicine, CA, United States.
  • Uri Nudel Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.
  • David Israeli Genethon, INSERM U-951, Evry, France.
  • Helen M. Blau Stanford University School of Medicine, Institute for Stem Cell Biology and Regenerative Medicine, Department of Microbiology and Immunology, Clinical Sciences Research Center, Stanford, CA, United States.
  • Asher Shainberg The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel.
  • Sara Neuman Ness-Ziona, Israel.
  • Gania Kessler-Icekson Laboratory of Cellular and Molecular Cardiology, Felsenstein Medical Research Center, Rabin Medical Center, Petah-Tikva, and Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel.
  • Erica Meghid Krull Easton, Massachusetts, United States.
  • Bruce Paterson Laboratory of Biochemistry and Molecular Biology, National Institutes of Health, Bethesda, Maryland, United States.
  • Ora Saxel Fuchs Rehovot, Israel.
  • David Greenberg Department of Biological Chemistry, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.
  • Rachel Sarig Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.
  • Orna Halevy Faculty of Agriculture, The Hebrew University, Rehovot, Israel.
  • Eijiro Ozawa National Institute of Neuroscience, NCNP, Tokyo, Japan.
  • Don J. Katcoff The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel.

It is with great sadness that we have learned about the passing of Professor David Yaffe (1929-2020, Israel). Yehi Zichro Baruch - May his memory be a blessing. David was a man of family, science and nature. A native of Israel, David grew up in the historic years that preceded the birth of the State of Israel. He was a member of the group that established Kibbutz Revivim in the Negev desert, and in 1948 participated in Israel’s War of Independence. David and Ruth eventually joined Kibbutz Givat Brenner by Rehovot, permitting David to be both a kibbutz member and a life-long researcher at the Weizmann Institute of Science, where David received his PhD in 1959. David returned to the Institute after his postdoc at Stanford. Here, after several years of researching a number of tissues as models for studying the process of differentiation, David entered the myogenesis field and stayed with it to his last day. With his dedication to the field of myogenesis and his commitment to furthering the understanding of the People and the Land of Israel throughout the international scientific community, David organized the first ever myogenesis meeting that took place in Shoresh, Israel in 1975. This was followed by the 1980 myogenesis meeting at the same place and many more outstanding meetings, all of which brought together myogenesis, nature and scenery. Herein, through the preparation and publication of this current manuscript, we are meeting once again at a “David Yaffe myogenesis meeting". Some of us have been members of the Yaffe lab, some of us have known David as his national and international colleagues in the myology field. One of our contributors has also known (and communicates here) about David Yaffe’s earlier years as a kibbutznick in the Negev. Our collective reflections are a tribute to Professor David Yaffe. We are fortunate that the European Journal of Translational Myology has provided us with tremendous input and a platform for holding this 2020 distance meeting "Farwell to Professor David Yaffe - A Pillar of the Myogenesis Field".


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Bar S, Barnea E, Levy Z, Neuman S, Yaffe D, Nudel U. A novel product of the Duchenne muscular dystrophy gene which greatly differs from the known isoforms in its structure and tissue distribution. Biochem J 1990;272:557-60. doi: 10.1042/bj2720557 DOI: https://doi.org/10.1042/bj2720557

Barnea E, Zuk D, Simantov R, Nudel U, Yaffe D. Specificity of expression of the muscle and brain dystrophin gene promoters in muscle and brain cells. Neuron 1990;5:881-8. doi: 10.1016/0896-6273(90)90348-j DOI: https://doi.org/10.1016/0896-6273(90)90348-J

den Dunnen JT, Casula L, Makover A, Bakker B, Yaffe D, Nudel U, van Ommen GJ. Mapping of dystrophin brain promoter: a deletion of this region is compatible with normal intellect. Neuromuscul Disord 1991;1(5):327-31. doi: 10.1016/0960-8966(91)90118-c DOI: https://doi.org/10.1016/0960-8966(91)90118-C

Makover A, Zuk D, Breakstone J, Yaffe D, Nudel U. Brain-type and muscle-type promoters of the dystrophin gene differ greatly in structure. Neuromuscul Disord 1991;1:39-45. doi: 10.1016/0960-8966(91)90041-p DOI: https://doi.org/10.1016/0960-8966(91)90041-P

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Rapaport D, Lederfein D, den Dunnen JT, Grootscholten PM, Van Ommen GJ, Fuchs O, Nudel U, Yaffe D. Characterization and cell type distribution of a novel, major transcript of the Duchenne muscular dystrophy gene. Differentiation 1992;49:187-93. doi: 10.1111/j.1432-0436.1992.tb00666.x DOI: https://doi.org/10.1111/j.1432-0436.1992.tb00666.x

Lederfein D, Levy Z, Augier N, Mornet D, Morris G, Fuchs O, Yaffe D, Nudel U. A 71-kilodalton protein is a major product of the Duchenne muscular dystrophy gene in brain and other nonmuscle tissues. Proc Natl Acad Sci U S A 1992;89:5346-50. doi: 10.1073/pnas.89.12.5346 DOI: https://doi.org/10.1073/pnas.89.12.5346

Rapaport D, Fuchs O, Nudel U, Yaffe D. Expression of the Duchenne muscular dystrophy gene products in embryonic stem cells and their differentiated derivatives. J Biol Chem 1992;267:21289-92 DOI: https://doi.org/10.1016/S0021-9258(19)36604-9

Rapaport D, Greenberg DS, Tal M, Yaffe D, Nudel U. Dp71, the nonmuscle product of the Duchenne muscular dystrophy gene is associated with the cell membrane. FEBS Lett 1993;328:197-202. doi: 10.1016/0014-5793(93)80992-4 DOI: https://doi.org/10.1016/0014-5793(93)80992-4

Lederfein D, Yaffe D, Nudel U. A housekeeping type promoter, located in the 3' region of the Duchenne muscular dystrophy gene, controls the expression of Dp71, a major product of the gene. Hum Mol Genet 1993;2:1883-8. doi: 10.1093/hmg/2.11.1883 DOI: https://doi.org/10.1093/hmg/2.11.1883

Prigojin H, Brusel M, Fuchs O, Shomrat R, Legum C, Nudel U, Yaffe D. Detection of Duchenne muscular dystrophy gene products in amniotic fluid and chorionic villus sampling cells. FEBS Lett 1993;335:223-30. doi: 10.1016/0014-5793(93)80734-c DOI: https://doi.org/10.1016/0014-5793(93)80734-C

Greenberg DS, Sunada Y, Campbell KP, Yaffe D, Nudel U. Exogenous Dp71 restores the levels of dystrophin associated proteins but does not alleviate muscle damage in mdx mice. Nat Genet 1994;8:340-4. doi: 10.1038/ng1294-340. DOI: https://doi.org/10.1038/ng1294-340

Greenberg DS, Schatz Y, Levy Z, Pizzo P, Yaffe D, Nudel U. Reduced levels of dystrophin associated proteins in the brains of mice deficient for Dp71. Hum Mol Genet 1996;5:1299-303. doi: 10.1093/hmg/5.9.1299 DOI: https://doi.org/10.1093/hmg/5.9.1299

Wang J, Pansky A, Venuti JM, Yaffe D, Nudel U. A sea urchin gene encoding dystrophin-related proteins. Hum Mol Genet 1998;7:581-8. doi: 10.1093/hmg/7.4.581 DOI: https://doi.org/10.1093/hmg/7.4.581

Sarig R, Mezger-Lallemand V, Gitelman I, Davis C, Fuchs O, Yaffe D, Nudel U. Targeted inactivation of Dp71, the major non-muscle product of the DMD gene: differential activity of the Dp71 promoter during development. Hum Mol Genet 1999;8:1-10. doi: 10.1093/hmg/8.1.1 DOI: https://doi.org/10.1093/hmg/8.1.1

Vilquin JT, Guérette B, Puymirat J, Yaffe D, Tomé FM, Fardeau M, Fiszman M, Schwartz K, Tremblay JP. Myoblast transplantations lead to the expression of the laminin alpha 2 chain in normal and dystrophic (dy/dy) mouse muscles. Gene Ther 1999;6:792-800. doi: 10.1038/sj.gt.3300889 DOI: https://doi.org/10.1038/sj.gt.3300889

Keshet GI, Bar-Peled O, Yaffe D, Nudel U, Gabizon R. The cellular prion protein colocalizes with the dystroglycan complex in the brain. J Neurochem 2000;75:1889-97. doi: 10.1046/j.1471-4159.2000.0751889.x. DOI: https://doi.org/10.1046/j.1471-4159.2000.0751889.x

Neuman S, Kaban A, Volk T, Yaffe D, Nudel U. The dystrophin / utrophin homologues in Drosophila and in sea urchin. Gene 2001;263:17-29. doi: 10.1016/s0378-1119(00)00584-9 DOI: https://doi.org/10.1016/S0378-1119(00)00584-9

Leibovitz S, Meshorer A, Fridman Y, Wieneke S, Jockusch H, Yaffe D, Nudel U. Exogenous Dp71 is a dominant negative competitor of dystrophin in skeletal muscle. Neuromuscul Disord 2002;12:836-44. doi: 10.1016/s0960-8966(02) 00141-4

Dalloz C, Sarig R, Fort P, Yaffe D, Bordais A, Pannicke T, Grosche J, Mornet D, Reichenbach A, Sahel J, Nudel U, Rendon A. Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mouse retina. Hum Mol Gene. 2003;12:1543-54. doi: 10.1093/hmg/ddg170 DOI: https://doi.org/10.1093/hmg/ddg170

de León MB, Montañez C, Gómez P, Morales-Lázaro SL, Tapia-Ramírez V, Valadez-Graham V, Recillas-Targa F, Yaffe D, Nudel U, Cisneros B. Dystrophin Dp71 expression is down-regulated during myogenesis: role of Sp1 and Sp3 on the Dp71 promoter activity. J Biol Chem 2005;280:5290-9. doi: 10.1074/jbc.M411571200. DOI: https://doi.org/10.1074/jbc.M411571200

Neuman S, Kovalio M, Yaffe D, Nudel U. The Drosophila homologue of the dystrophin gene - introns containing promoters are the major contributors to the large size of the gene. FEBS Lett. 2005;579:5365-71. doi: 10.1016/j.febslet.2005.08.073. DOI: https://doi.org/10.1016/j.febslet.2005.08.073

Bermúdez de León M, Montañez C, Gómez P, Luz Morales-Lázaro S, Tapia-Ramírez V, Valadez-Graham V, Recillas-Targa F, Yaffe D, Nudel U, Cisneros B. Dystrophin Dp71 expression is down-regulated during myogenesis: role of Sp1 and Sp3 on the Dp71 promoter activity. J Biol Chem 2005;280:5290-9. doi: 10.1074/jbc.M411571200 DOI: https://doi.org/10.1074/jbc.M411571200

Sarig R, Baruchi Z, Fuchs O, Nudel U, Yaffe D. Regeneration and transdifferentiation potential of muscle-derived stem cells propagated as myospheres. Stem Cells 2006;24:1769-78. doi: 10.1634/stemcells.2005-0547 DOI: https://doi.org/10.1634/stemcells.2005-0547

Shcherbata HR, Yatsenko AS, Patterson L, Sood VD, Nudel U, Yaffe D, Baker D, Ruohola-Baker H. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J. 2007;26:481-93. doi: 10.1038/sj.emboj.7601503. DOI: https://doi.org/10.1038/sj.emboj.7601503

Taghli-Lamallem O, Akasaka T, Hogg G, Nudel U, Yaffe D, Chamberlain JS, Ocorr K, Bodmer R. Dystrophin deficiency in Drosophila reduces lifespan and causes a dilated cardiomyopathy phenotype. Aging Cell 2008;7:237-49. doi: 10.1111/j.1474-9726.2008.00367.x. DOI: https://doi.org/10.1111/j.1474-9726.2008.00367.x

Fort PE, Sene A, Pannicke T, Roux MJ, Forster V, Mornet D, Nudel U, Yaffe D, Reichenbach A, Sahel JA, Rendon A. Kir4.1 and AQP4 associate with Dp71- and utrophin-DAPs complexes in specific and defined microdomains of Müller retinal glial cell membrane. Glia 2008 Apr 15;56(6):597-610. doi: 10.1002/glia.20633 DOI: https://doi.org/10.1002/glia.20633

Daoud F, Candelario-Martínez A, Billard JM, Avital A, Khelfaoui M, Rozenvald Y, Guegan M, Mornet D, Jaillard D, Nudel U, Chelly J, Martínez-Rojas D, Laroche S, Yaffe D, Vaillend C. Role of mental retardation-associated dystrophin-gene product Dp71 in excitatory synapse organization, synaptic plasticity and behavioral functions. PLoS One 2008;4:e6574. doi: 10.1371/journal.pone.0006574 DOI: https://doi.org/10.1371/journal.pone.0006574

Aharoni R, Aizman E, Fuchs O, Arnon R, Yaffe D, Sarig R. Transplanted myogenic progenitor cells express neuronal markers in the CNS and ameliorate disease in experimental autoimmune encephalomyelitis. J Neuroimmunol 2009;215:73-83. doi: 10.1016/j.jneuroim.2009.08.009. DOI: https://doi.org/10.1016/j.jneuroim.2009.08.009

Sarig R, Fuchs O, Tencer L, Panski A, Nudel U, Yaffe D. Cloned myogenic cells can transdifferentiate in vivo into neuron-like cells. PLoS One. 2010;5:e8814. doi: 10.1371/journal.pone.0008814. DOI: https://doi.org/10.1371/journal.pone.0008814

Benabdesselam R, Sene A, Raison D, Benmessaoud-Mesbah O, Ayad G, Mornet D, Yaffe D, Rendon A, Hardin-Pouzet H, Dorbani-Mamine L. A deficit of brain dystrophin 71 impairs hypothalamic osmostat. J Neurosci Res 2010;88:324-34. doi: 10.1002/jnr.22198. DOI: https://doi.org/10.1002/jnr.22198

Dadon-Nachum M, Ben-Zur T, Srugo I, Shamir HM, Melamed E, Yaffe D, Offen D. Therapeutic effect of myogenic cells modified to express neurotrophic factors in a rat model of sciatic nerve injury. J Stem Cells Regen Med 2012;8:21-7. doi: 10.46582/jsrm.0801004. DOI: https://doi.org/10.46582/jsrm.0801004

Dadon-Nachum M, Ben-Yaacov K, Ben-Zur T, Barhum Y, Yaffe D, Perlson E, Offen D. Transplanted modified muscle progenitor cells expressing a mixture of neurotrophic factors delay disease onset and enhance survival in the SOD1 mouse model of ALS. J Mol Neurosci 2015;55:788-97. doi: 10.1007/s12031-014-0426-0. DOI: https://doi.org/10.1007/s12031-014-0426-0

Glat MJ, Benninger F, Barhum Y, Ben-Zur T, Kogan E, Steiner I, Yaffe D, Offen D. Ectopic Muscle Expression of Neurotrophic Factors Improves Recovery After Nerve Injury. J Mol Neurosci 2016;58:39-45. doi: 10.1007/s12031-015-0648-9. DOI: https://doi.org/10.1007/s12031-015-0648-9

Guy R, Grynspan F, Ben-Zur T, Panski A, Lamdan R, Danon U, Yaffe D, Offen D. Human muscle progenitor cells overexpressing neurotrophic factors improve neuronal regeneration in a sciatic nerve injury mouse model. Front Neurosci 2019;13:151. doi: 10.3389/fnins.2019.00151. DOI: https://doi.org/10.3389/fnins.2019.00151

Kern H, Boncompagni S, Rossini K, Mayr W, Fanò G, Zanin ME, Podhorska-Okolow M, Protasi F, Carraro U. Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus, which is reversible by functional electrical stimulation (FES): a role for myofiber regeneration? J Neuropathol Exp Neurol. 2004;63:919-31. doi: 10.1093/jnen/63.9.919. DOI: https://doi.org/10.1093/jnen/63.9.919

Carraro U, Kern H. Severely atrophic human muscle fibers with nuclear misplacement survive many years of permanent denervation. Eur J Transl Myol 2016;26(2):5894. doi: 10.4081/ejtm.2016.5894 DOI: https://doi.org/10.4081/ejtm.2016.5894

Kern H. Carraro U. Home-based functional electrical stimulation of human permanent denervated muscles: A narrative review on diagnostics, managements, results and byproducts Revisited 2020. Diagnostics 2020;10, 529. doi: 10.3390/diagnostics10080529 DOI: https://doi.org/10.3390/diagnostics10080529

Some of the biographical information in this paragraph and the images in Figs 1 and 3 are from a PDF found online “The Graduates”, published by the Weizmann Institute of Science, celebrating 50 years of excellent of its Feinberg Graduate School (published ~2008). https://wis-wander.Weizmann.ac.il/sites/default/files/images/Books/The%20Graduates.pdf Additional biographical details were contributed by Dr. Gania Kessler-Icekson.

EMBO workshop on muscle cell culture in the study of gene expression during differentiation, Shoresh, Israel 1975.

EMBO Workshop on Myogenesis and Molecular Genesis of Muscle Diseases. Ein-Gedi, Israel, 1996.

Yablonka-Reuveni, Z., Stockdale, F., Nudel, U., Israeli, D., Blau, H. M., Shainberg, A., Neuman, S., Kessler-Icekson, G., Meghid Krull, E., Paterson, B., Saxel Fuchs, O., Greenberg, D., Sarig, R., Halevy, O., Ozawa, E., & Katcoff, D. J. (2020). Farewell to Professor David Yaffe – A Pillar of the Myogenesis Field. European Journal of Translational Myology, 30(3). https://doi.org/10.4081/ejtm.2020.9306

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