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Hous-Whipple Award Hous-Whipple Award The Rous-Whipple Award was established by the American Society for Investigative Pathology to recognize a career of outstanding scientific contribution. The 1994 recipient of the Rous-Whipple Award, Dr. Nicholas K. Gonatas, delivered a lecture entitled "Contributions to the Physiology and Pathology of the Golgi Apparatus" after the presentation of the award on Tuesday, April 26, 1994 in Anaheim, California, at the meeting of the Federation of American Societies for Experimental Biology. Americanc journal ofPathology, Vol. 145, No. 4. October 1994 Copyright ) Amenican Society for Investigative Pathology Rous-Whipple Award Lecture Contributions to the Physiology and Pathology of the Golgi Apparatus Nicholas K. Gonatas am honored to receive this award named after Pey- From the Department ofPathology and Laboratory ton Rous and George Whipple, eminent pathologists Medicine, Division ofNeuropathology, University qf and Nobel laureates for their fundamental discoveries Pennsylvania School ofMedicine, on tumor-inducing viruses and vitamins, respectively. Philadelphia, Pennsylvania As we are approaching the 1 00th anniversary of the discovery of the Golgi apparatus by Camillo Golgi 0 BLo' f3pasXv;, TJ he TEXVT1 /IrKpT. (1844-1926), professor of histology and general pa- "The life is short, the craft is long. " thology at the university of Pavia, we should be re- Hippocrates, c. 460-3 73 B.C. minded that for a long time the status of this important Aphorisms organelle was controversial. Until the late forties, the Golgi apparatus-complex was considered by many cytologists as an artifact of fixation and tissue processing.1 Over the last 40 years The importance of the Golgi apparatus in the the status of the Golgi apparatus has been upgraded transport, processing, and targeting ofproteins from artifact to "center stage," which is not an exag- destinedfor secretion, plasma membranes, and gerated characterization considering the central lysosomes has emergedfrom numerous studies. roles of the organelle in the transport, processing, and In this paper we review studies from our labo- targeting of polypeptides destined for secretion, ratory dealing with 1) the Golgi apparatus during plasma membranes, or lysosomes.1 In addition to the mitosis and the role ofmicrotubules in maintain- above centrifugal functions, the Golgi apparatus, and ing the structure ofthe organeUe, 2) the endocy- more precisely GERL or TGN, is involved in the ret- tosis ofantibodies, exogenous lectins, and toxins rograde or centripetal transport of antibodies, lectins into the Golgi apparatus ofseveral cells including and toxins.2 4 neurons in vivo and in vitro, 3) the traffic ofMG- Many of the studies to be reviewed here were per- 160, a membrane sialoglycoprotein ofthe medial formed by Jacqueline Gonatas and Anna Stieber of cisternae ofthe Golgi apparatus,from the trans- our laboratory, who over the last 25 years have de- Golgi network to the Golgi cisternae, and 4) the voted their energies, insights, skills, and experience involvement ofthe Golgi apparatus ofmotor neu- in cellular and molecular studies on the Golgi appa- rons in the pathogenesis of amyotrophic lateral ratus. Recent collaborators are Zissimos Mourelatos, sclerosis. We conclude with a summary ofongoing Kate Johnston, and Jun Chen, who contributed to work on the primary structure of MG-160 and studies on the retrograde traffic and cDNA sequenc- introduce evidence suggesting that this intrinsic ing of MG-160. An important collaborator to our recent membrane protein of the Golgi apparatus may studies has been the late Becca Fleischer who shared be involved in the regulation of endogenous, with us her enormous knowledge and vast experi- autocrine, basic fibroblast growth factor. We ence in the enzymology and cell biology of the Golgi hope that this review will stimulate studies on the Golgi apparatus which lead ofneurons, may Supported by National Institutes of Health grant NS-05572. to the discovery ofneuron-specific properties of Accepted for publication July 11, 1994. this organeUe and its involvement in important Address reprint requests to Nicholas K. Gonatas, 418 Johnson the pathogenesis of neurodegenerative disor- Pavillion, University of Pennsylvania School of Medicine, Philadel- ders. (AmJPathol 1994, 145:751-761) phia, PA 19104. 751 752 Gonatas AJP October 1994, Vol. 145, No. 4 apparatus. Her untimely death has deprived the com- gous" to spindle tubules, and not elements of the en- munity of cell-molecular biologists of the Golgi ap- doplasmic reticulum as it was previously claimed. paratus of a highly original scientist who has made classic contributions to the field. Ongoing research on the Golgi apparatus is volu- The Endocytosis of Antibodies, minous and in "full effervescence." Due to the nature Exogenous Lectins, and Toxins in the of this presentation only a few relevant contributions Golgi Apparatus from other laboratories will be discussed. Summaries of the results will be presented under Review of Pre- Two important methodologic innovations made pos- vious Studies, while brief discussions of the signifi- sible these studies. The first was the method for the cance of the results will be presented under Impli- light and electron microscopic visualization of horse- cations and Future Directions. radish peroxidase (HRP), introduced by Graham and Karnovsky.8 The second were the methods, intro- duced by Avrameas and Ternynck,9-1 1 for the prepa- ration of immunoadsorbents and the covalent conju- Review of Previous Studies gation of HRP with antibodies and lectins. These studies were conducted both in vitro using The Golgi Apparatus during Mitosis and cultured rat neurons, rat pheochromocytoma (PC12) the Role of Microtubules in Maintaining cells, murine neuroblastoma cells, mouse or rat lym- the Structure of the Organelle phoid cells, and cultured human fibroblasts, and in vivo, using injections of ligands into rat brains, eyes, was introduced to cell biology by Elliott Robbins. In and submandibular glands. our first study, published in 1964, we examined by transmission electron microscopy and cytochemical In vitro studies techniques for acid phosphatase and thiamine pyro- In the first of these studies, we observed that phosphatase HeLa cells during various stages of mi- peroxidase-labeled antibodies against IgG were in- tosis.5 This paper has been a standard reference to ternalized in clusters of tubules resembling the Golgi students of mitosis over more than a quarter of a cen- apparatus in rat and mouse plasma cells. On retro- tury (ISI, Current Contents, Life Sciences, September spect, these compartments probably corresponded 25, 1989, vol. 32, no. 39). In this study, we were im- to GERL (Golgi-endoplasmic reticulum-lysosome) pressed by the apparent "disappearance" of the or TGN (the trans-Golgi network).2'12'13 Originally, Golgi apparatus during early prophase and its Novikoff and Novikoff,12 using the cytochemical prompt "reappearance" in telophase.5 Furthermore, techniques for thiamine pyrophosphatase and acid in prophase the diffuse network of the normally phosphatase, had identified a system of acid present cytoplasmic microtubules disappeared, phosphatase-positive tubules, vesicles, and cister- while simultaneously the lysosomes were aggregated nae at the mature or trans aspect of the Golgi appa- in peripherally located clusters. This observation led ratus which they named GERL, for Golgi apparatus- us to examine the effect of the microtubule-disrupting Endoplasmic Reticulum-Lysosome. They postulated agent colchicine on interphase HeLa cells.6 Under that GERL served as a direct conduit of molecules the influence of colchicine, the Golgi apparatus of in- from the rough endoplasmic reticulum (RER) to the terphase cells fragmented while the lysosomes were lysosomes. A few years later, Griffiths and Simons13 distributed in circumferential clusters similar to those renamed GERL as TGN for trans Golgi network, and seen in mitotic cells.6 We attributed the "disappear- proposed that TGN serves as the common site of exit ance" of the Golgi apparatus during mitosis and the of all proteins processed through the Golgi appara- fragmentation of the organelle in colchicine-treated tus. cells to the same cause, namely to the disruption of Conclusive evidence for the existence of a retro- microtubules, which in mitotic cells occurs physi- grade pathway between cell surface receptors to Ii- ologically and in interphase cells after treatment with gands and the Golgi apparatus was provided by two colchicine.6 experiments involving the internalization of Perhaps one of the most important findings of these peroxidase-labeled ricin and wheat germ agglutinin early studies was the realization that axons contained in cultured neurons.34 In subsequent studies, per- microtubules or "neurotubules" as we called them. In formed with cultured neurons, neuroblastoma, rat a paper, also published in 1964,7 we showed that ax- pheochromocytoma (PC12) and lymphoid cells, we ons and dendrites contained structures "homolo- confirmed the existence of a retrograde pathway of Rous-Whipple Award Lecture 753 AJP October 1994, Vol. 145, No. 4 endocytosis into GERL-TGN of ligands with affinities to several cell surface receptors.14-24 The endocy- tosis was specifically inhibited when the ligands were incubated with soluble receptors, namely, D-galactose with ricin, N-acetylglucosamine with wheat germ agglutinin, and GM1 ganglioside with cholera toxin.4'11'15'16 Furthermore, in cells deficient for the receptor
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