Proteomics Identifies Golgi phosphoprotein 3 (GOLPH3) with A Link Between Golgi Structure, Cancer, DNA Damage and Protection from Cell Death

GOLPH3 is the first example of a Golgi resident oncogene protein. It was independently identified in multiple screens; first in proteomic-based screens as a resident protein of the Golgi apparatus, and second as an oncogene product in a screen for genes amplified in cancer. A third screen uncovered the association of GOLPH3 with the Golgi resident phospholipid, phosphatidyl inositol 4 phosphate (PI4P) to maintain the characteristic ribbon structure of the Golgi apparatus favoring vesicular transport of secretory proteins. GOLPH3 is the first example of a Golgi resident oncogene protein. It was independently identified in multiple screens; first in proteomic-based screens as a resident protein of the Golgi apparatus, and second as an oncogene product in a screen for genes amplified in cancer. A third screen uncovered the association of GOLPH3 with the Golgi resident phospholipid, phosphatidyl inositol 4 phosphate (PI4P) to maintain the characteristic ribbon structure of the Golgi apparatus favoring vesicular transport of secretory proteins. The organization of the Golgi apparatus is unique to each cell type of every organ in the body. In many cell types it consists of stacks of cisternae connected by membranous tubules and defined as the Golgi ribbon (1.Rambourg A. Clermont Y. Hermo L. Three-dimensional architecture of the golgi apparatus in Sertoli cells of the rat.Am. J. Anat. 1979; 154: 455-476Crossref PubMed Scopus (151) Google Scholar). Although somehow linked to its central role in coordinating the process of protein secretion, a mechanistic rationale for the basic structure of the Golgi apparatus has eluded cell biologists (2.Emr S. Glick B.S. Linstedt A.D. Lippincott-Schwartz J. Luini A. Malhotra V. Marsh B.J. Nakano A. Pfeffer S.R. Rabouille C. Rothman J.E. Warren G. Wieland F.T. Journeys through the Golgi–taking stock in a new era.J. Cell Biol. 2009; 187: 449-453Crossref PubMed Scopus (135) Google Scholar). Proteomics has provided an unprecedented window into the protein makeup of the Golgi apparatus that is slowly resolving the puzzle of its structure and functions (3.Gilchrist A. Au C.E. Hiding J. Bell A.W. Fernandez-Rodriguez J. Lesimple S. Nagaya H. Roy L. Gosline S.J. Hallett M. Paiement J. Kearney R.E. Nilsson T. Bergeron J.J. Quantitative proteomics analysis of the secretory pathway.Cell. 2006; 127: 1265-1281Abstract Full Text Full Text PDF PubMed Scopus (385) Google Scholar, 4.Au C.E. Hermo L. Byrne E. Smirle J. Fazel A. Simon P.H. Kearney R.E. Cameron P.H. Smith C.E. Vali H. Fernandez-Rodriguez J. Ma K. Nilsson T. Bergeron J.J. Expression, sorting, and segregation of Golgi proteins during germ cell differentiation in the testis.Mol. Biol. Cell. 2015; 26: 4015-4032Crossref PubMed Scopus (21) Google Scholar, 5.Au C.E. Hermo L. Byrne E. Smirle J. Fazel A. Kearney R.E. Smith C.E. Vali H. Fernandez-Rodriguez J. Simon P.H. Mandato C. Nilsson T. Bergeron J.J. Compartmentalization of membrane trafficking, glucose transport, glycolysis, actin, tubulin and the proteasome in the cytoplasmic droplet/Hermes body of epididymal sperm.Open Biol. 2015; 5: 150080Crossref PubMed Scopus (23) Google Scholar). Early efforts that characterized abundant proteins of isolated Golgi fractions by mass spectrometry (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar) led to the discovery of a previously unreported protein named GPP34 1The abbreviations used are: GPP34; golgi peripheral protein of 34kDa; ADAM10, A disintegrin and metalloprotease 10; COPI, coatomer protein complex I; DNA-PK, DNA protein kinase; EST, expressed sequence tags; FAM3C, family with sequence similarity 3; GMX33, golgi matrix protein of 33kDa; GOLPH, golgi phosphoprotein; HTRA1, high temperature requirement A1 serine protease; MALDI, matrix-assisted laser desorption/ionization; MMP1, matrix metallopeptidase 1; mTOR, mechanistic target of rapamycin; PDGFA, platelet derived growth factor subunit A; PI4P, phosphatidyl inositol 4- phosphate; PITPNC1, phosphoinositide transfer protein, cytoplasmic 1; RAB, Ras in the brain GTPase; SAC1, suppressor of the temperature-conditional act1–1 allele; SDS PAGE, sodium dodecyl sulphate polyacrylamide gel electrophoresis; VPS, vacuolar protein sorting. 1The abbreviations used are: GPP34; golgi peripheral protein of 34kDa; ADAM10, A disintegrin and metalloprotease 10; COPI, coatomer protein complex I; DNA-PK, DNA protein kinase; EST, expressed sequence tags; FAM3C, family with sequence similarity 3; GMX33, golgi matrix protein of 33kDa; GOLPH, golgi phosphoprotein; HTRA1, high temperature requirement A1 serine protease; MALDI, matrix-assisted laser desorption/ionization; MMP1, matrix metallopeptidase 1; mTOR, mechanistic target of rapamycin; PDGFA, platelet derived growth factor subunit A; PI4P, phosphatidyl inositol 4- phosphate; PITPNC1, phosphoinositide transfer protein, cytoplasmic 1; RAB, Ras in the brain GTPase; SAC1, suppressor of the temperature-conditional act1–1 allele; SDS PAGE, sodium dodecyl sulphate polyacrylamide gel electrophoresis; VPS, vacuolar protein sorting.for Golgi Peripheral Protein of 34 kDa. Renamed GOLPH3 (GOLgi PHosphoprotein3), studies of its function have provided mechanistic insight into Golgi apparatus structure and cell homeostasis that may be informative for strategies to unravel the functions of the thousands of proteins discovered by -omics technologies (7.Gaudet P. Michel P.A. Zahn-Zabal M. Britan A. Cusin I. Domagalski M. Duek P.D. Gateau A. Gleizes A. Hinard V. de Laval V.R. Lin J. Nikitin F. Schaeffer M. Teixeira D. Lane L. Bairoch A. The neXtProt knowledgebase on human proteins: 2017 update.Nucleic Acids Res. 2016; 45: D177-D182Crossref PubMed Scopus (123) Google Scholar). GOLPH3 was first characterized in a proteomics screen of highly enriched Golgi fractions (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar). Detailed electron microscope morphometry of liver parenchymal cells in situ, had revealed that the Golgi accounted for only 1% of the volume of the hepatocyte (8.Blouin A. Bolender R.P. Weibel E.R. Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. A stereological study.J. Cell Biol. 1977; 72: 441-455Crossref PubMed Scopus (599) Google Scholar). Therefore, isolation of the Golgi apparatus from rat liver homogenates (Fig. 1) was necessary to assure the characterization of Golgi resident proteins given the low dynamic range and low sensitivity of mass spectrometry at that time. To enrich further for Golgi membrane proteins, phase partitioning of the isolated Golgi fraction with the detergent Triton X-114 was performed to select for membrane proteins (9.Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution.J. Biol. Chem. 1981; 256: 1604-1607Abstract Full Text PDF PubMed Google Scholar), then followed by protein separation through SDS-PAGE (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar). Eighty-one proteins were characterized by mass spectrometry (MALDI and nanoelectrospray MS/MS) complemented by N-terminal sequencing (Edman degradation); of these 24 were contaminants. As expected, most of the 57 genuine Golgi proteins revealed primary sequences with transmembrane domains or known lipid anchors. However, one protein that was named GPP34 (GOLPH3) had not been characterized previously. By both immunofluorescence and analytical subcellular fractionation, GOLPH3 was localized to the Golgi apparatus and cytosol. By cryo-immuno electron microscopy, gold-labeled antibodies revealed GOLPH3 localization at the periphery of isolated stacked Golgi cisternae (Fig. 1) (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar). The complete protein sequence of GOLPH3 was inferred from database searches (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar). Initially, a perfect match of the sequence of one tryptic fragment was found in the human EST database corresponding to a previously unidentified protein that was identified as GOLPH3 (Fig. 1). The complete sequence of GOLPH3 corresponded to 2 human gene products, 2 mouse gene products and one gene product in D. melanogaster fruit flies, the worm C. elegans, and the budding yeast S. cerevisiae. There were no motifs or transmembrane domains to explain the localization of GOLPH3 to the Golgi or its partitioning into the detergent phase of Triton X-114. Wu et al. coincidentally discovered a protein they named GMX33 (10.Wu C.C. Taylor R.S. Lane D.R. Ladinsky M.S. Weisz J.A. Howell K.E. GMx33: a novel family of trans-Golgi proteins identified by proteomics.Traffic. 2000; 1: 963-975PubMed Google Scholar) as a Golgi matrix protein (hence GMX) of identical sequence to GOLPH3. GMX33 was also found to partition into Triton-X-114 and further characterized as a phosphoprotein. This was deduced from multiple spots for GMX33 on 2D gels that resolved into one after alkaline phosphatase treatment (10.Wu C.C. Taylor R.S. Lane D.R. Ladinsky M.S. Weisz J.A. Howell K.E. GMx33: a novel family of trans-Golgi proteins identified by proteomics.Traffic. 2000; 1: 963-975PubMed Google Scholar). One of the 2 gene products for GOLPH3 in mice and humans corresponded to a related sequence but different gene product (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar, 10.Wu C.C. Taylor R.S. Lane D.R. Ladinsky M.S. Weisz J.A. Howell K.E. GMx33: a novel family of trans-Golgi proteins identified by proteomics.Traffic. 2000; 1: 963-975PubMed Google Scholar) named GOLPH3L. In human cells, GOLPH3L reveals 68% identity and 78% similarity in primary sequence to GOLPH3. Furthermore expression of GOLPH3L is restricted to a subset of secretory cell types with a function deduced to be antagonistic to GOLPH3 in these cell types (e.g. (11.Ng M.M. Dippold H.C. Buschman M.D. Noakes C.J. Field S.J. GOLPH3L antagonizes GOLPH3 to determine Golgi morphology.Mol. Biol. Cell. 2013; 24: 796-808Crossref PubMed Scopus (55) Google Scholar)). This review will focus on GOLPH3. Both Bell et al. (6.Bell A.W. Ward M.A. Blackstock W.P. Freeman H.N. Choudhary J.S. Lewis A.P. Chotai D. Fazel A. Gushue J.N. Paiement J. Palcy S. Chevet E. Lafreniere-Roula M. Solari R. Thomas D.Y. Rowley A. Bergeron J.J. Proteomics characterization of abundant Golgi membrane proteins.J. Biol. Chem. 2001; 276: 5152-5165Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar) and Wu et al. (10.Wu C.C. Taylor R.S. Lane D.R. Ladinsky M.S. Weisz J.A. Howell K.E. GMx33: a novel family of trans-Golgi proteins identified by proteomics.Traffic. 2000; 1: 963-975PubMed Google Scholar) found a similarity between the primary sequence of mammalian GOLPH3 and the predicted yeast protein Vps74p. Budding yeast are a powerful model system to solve the mechanisms of proteins linked to the secretory pathway (12.Schekman R. Sudhof T. An interview with Randy Schekman and Thomas Sudhof.Trends Cell Biol. 2014; 24: 6-8Abstract Full Text Full Text PDF PubMed Google Scholar). Through yeast genetics, the first functions of GOLPH3 were deduced. In 2008, Schmitz et al. (13.Schmitz K.R. Liu J. Li S. Setty T.G. Wood C.S. Burd C.G. Ferguson K.M. Golgi localization of glycosyltransferases requires a Cell. 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The proteins with sequence similarity A1 serine derived growth factor subunit and were for the of cells through the matrix for and for cells to the in of and after of MMP1, HTRA1, PDGFA, or in cells from Field S.J. of at the Cell Biol. 45: PubMed Scopus Google in a new The of et al. K. H. K. to the golgi to Cell. 2016; Full Text Full Text PDF PubMed Scopus Google Scholar) reveals an to that of et al. Dippold H.C. Buschman M.D. M. Noakes C.J. J. M.M. J. H. Field S.J. DNA Golgi and 2014; Full Text Full Text PDF PubMed Scopus Google Scholar) is in on the Golgi by of the gene ribbon and in cells and of the GOLPH3 gene Golgi stacks and in are each linked to cancer. The may with the from DNA and cell Field S.J. of at the Cell Biol. 45: PubMed Scopus Google Scholar). for the of gene amplified GOLPH3 have been R. S. G. Luini A. GOLPH3 and is the Cell. 2016; PubMed Scopus Google Scholar), the of GOLPH3 to and through E. V. Wu J. S. Wu M. S. T. J. A. Y. A. L. GOLPH3 and sensitivity in 2009; PubMed Scopus Google Scholar). It has also been that GOLPH3 gene in to of Golgi R. S. G. Luini A. GOLPH3 and is the Cell. 2016; PubMed Scopus Google Scholar). The is that the of of protein through the Golgi vesicular transport to the cell the of secretory proteins be linked to cancer. GOLPH3 expression during cell differentiation C.E. Hermo L. Byrne E. Smirle J. Fazel A. Simon P.H. Kearney R.E. Cameron P.H. Smith C.E. Vali H. Fernandez-Rodriguez J. Ma K. Nilsson T. Bergeron J.J. Expression, sorting, and segregation of Golgi proteins during germ cell differentiation in the testis.Mol. Biol. Cell. 2015; 26: 4015-4032Crossref PubMed Scopus (21) Google Scholar) is the the secretory product of germ It is during that the Golgi ribbon is at its most A of expression is also at the of from the There is no Golgi ribbon in only Golgi cisternae are C.E. Hermo L. Byrne E. Smirle J. Fazel A. Simon P.H. Kearney R.E. Cameron P.H. Smith C.E. Vali H. Fernandez-Rodriguez J. Ma K. Nilsson T. Bergeron J.J. Expression, sorting, and segregation of Golgi proteins during germ cell differentiation in the testis.Mol. Biol. Cell. 2015; 26: 4015-4032Crossref PubMed Scopus (21) Google Scholar) to Golgi apparatus structure in budding yeast E. J. B.J. Glick B.S. Golgi in 2006; PubMed Scopus Google Scholar)). Although the high expression of GOLPH3 during is (Fig. the function of GOLPH3 in is as in et al. S. G. G. V. A. GOLPH3 is for and localization to the during in 2014; PubMed Scopus Google Scholar) uncovered a new function for GOLPH3. GOLPH3 localization to the Golgi and the of It was that linked to GOLPH3 and a at the for and at studies have been S. A. R. L. M. G. A. with GOLPH3 and Golgi structure and during in Biol. PubMed Scopus (23) Google Scholar) to in the requirement of the for GOLPH3 to Golgi apparatus as K. H. K. to the golgi to Cell. 2016; Full Text Full Text PDF PubMed Scopus Google and the during S. A. R. L. M. G. A. with GOLPH3 and Golgi structure and during in Biol. PubMed Scopus (23) Google Scholar). new function of GOLPH3 may be related to the requirement of to the that the of these is necessary for to be as C.E. Hermo L. Byrne E. Smirle J. Fazel A. Simon P.H. Kearney R.E. Cameron P.H. Smith C.E. Vali H. Fernandez-Rodriguez J. Ma K. Nilsson T. Bergeron J.J. Expression, sorting, and segregation of Golgi proteins during germ cell differentiation in the testis.Mol. Biol. Cell. 2015; 26: 4015-4032Crossref PubMed Scopus (21) Google Scholar). function for GOLPH3 has been in the of Golgi apparatus to the of cells by membrane and M. K. Field S.J. GOLPH3 cell by Golgi and to the Biol. Cell. 2016; PubMed Scopus Google Scholar). the protein to its The between the Golgi structure and function has on the role of the Golgi ribbon in mammalian The on the Golgi to the Golgi ribbon are K. K. J.A. the of and in Golgi Scopus Google Scholar). GOLPH3 on the Golgi ribbon may of the by cell biologists by the Golgi apparatus structure (2.Emr S. Glick B.S. Linstedt A.D. Lippincott-Schwartz J. Luini A. Malhotra V. Marsh B.J. Nakano A. Pfeffer S.R. Rabouille C. Rothman J.E. Warren G. Wieland F.T. Journeys through the Golgi–taking stock in a new era.J. Cell Biol. 2009; 187: 449-453Crossref PubMed Scopus (135) Google of GOLPH3. of functions deduced for for Golgi localization of in budding K.R. Liu J. Li S. Setty T.G. Wood C.S. Burd C.G. Ferguson K.M. Golgi localization of glycosyltransferases requires a Cell. Full Text Full Text PDF PubMed Scopus Google Scholar, L. L. dynamic of glycosyltransferases in the PubMed Scopus Google Scholar, L. L. A N-terminal in proteins to PubMed Scopus Google Scholar, C.S. C.S. C.J. C.J. V. Ferguson K.M. Burd C.G. of in the Golgi apparatus by and phosphoinositide Biol. Cell. PubMed Scopus Google with Golgi in budding yeast and mammalian H.C. M.M. R. P.A. S. T. H. Field S.J. GOLPH3 and to and the Golgi to 2009; Full Text Full Text PDF PubMed Scopus Google Scholar, C.S. Schmitz K.R. Setty T.G. Ferguson K.M. Burd C.G. by to Golgi Cell Biol. 2009; 187: PubMed Scopus Google structure of Golgi ribbon in mammalian cells and of H.C. M.M. R. P.A. S. T. H. Field S.J. GOLPH3 and to and the Golgi to 2009; Full Text Full Text PDF PubMed Scopus Google Scholar, Dippold H.C. Buschman M.D. M. Noakes C.J. J. M.M. J. H. Field S.J. DNA Golgi and 2014; Full Text Full Text PDF PubMed Scopus Google Scholar, K. H. K. to the golgi to Cell. 2016; Full Text Full Text PDF PubMed Scopus Google amplified and to be an oncogene in human E. V. Wu J. S. Wu M. S. T. J. A. Y. A. L. GOLPH3 and sensitivity in 2009; PubMed Scopus Google Scholar, M.D. J. Field S.J. GOLPH3 the DNA and Res. 2015; PubMed Scopus Google Scholar, L. from the mechanisms and for Golgi Res. PubMed Scopus Google by DNA Protein to of Golgi ribbon and from cell to DNA Dippold H.C. Buschman M.D. M. Noakes C.J. J. M.M. J. H. Field S.J. DNA Golgi and 2014; Full Text Full Text PDF PubMed Scopus Google Scholar) in a new Through of Golgi liver fractions by different GOLPH3 was discovered through as a Golgi resident protein, multiple from screens to complete of its in cell function and to cancer.

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