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Outgrowth and Protein Synthesis by Pc12 Cells As a Function of Substratum and Nerve Growth Factor’

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Outgrowth and Protein Synthesis by Pc12 Cells As a Function of Substratum and Nerve Growth Factor’ 0270~6474/82/0208-1157$02.00/O The Journal of Neuroscience Copyright 0 Society for Neuroscience Vol. 2, No. 8, pp. 1157-1175 Printed in U.S.A. August 1982 NEURITE OUTGROWTH AND PROTEIN SYNTHESIS BY PC12 CELLS AS A FUNCTION OF SUBSTRATUM AND NERVE GROWTH FACTOR’ DENNIS K. FUJII, SHARON L. MASSOGLIA, NAPHTALI SAVION, AND DENIS GOSPODAROWICZ’ Cancer Research Institute and the Departments of Medicine and Ophthalmology, University of California Medical Center, San Francisco, California 94143 Received November 16, 1981; Revised March 11, 1982; Accepted March 26, 1982 Abstract Numerous studies have implied that enhanced cell-substratum adhesion plays a role in neurite outgrowth by neuronal cells. Using an extracellular matrix (ECM) produced by cultured corneal endothelial cells, we have investigated attachment and de novo neurite outgrowth by the pheochro- mocytoma cell line, PC12. PC12 cells were found to attach more rapidly and efficiently to the ECM than to plastic or collagen-coated surfaces. An extensive but temporary (5 to lo-day) neurite outgrowth occurred in the absence of nerve growth factor (NGF) when cells were on the ECM. However, long term neurite survival and further elongation required NGF. Our findings are consistent with the hypothesis that protein(s) in the ECM has an important role in neurite outgrowth. Thus, NGF may not so much initiate neurite outgrowth as it stabilizes neurites. ECM and NGF also were found to modulate cellular protein synthesis by PC12 cells. On ECM, a decreased synthesis of many high molecular weight proteins (ikfr > 85,000) was observed in comparison to that of cells on collagen-coated dishes. The presence of neurites (in the presence or absence of NGF) was associated with the induction of the synthesis of a cellular protein (&ir = 55,000 to 56,000 and p1 of 5.6). NGF was found to increase markedly the synthesis of two secreted proteins, while it drastically reduced the synthesis of all others regardless of the substratum upon which the cells were maintained. Among the various factors which can influence axonal strata that they encounter during the elongation process growth in vivo are chemotactic and/or trophic factors, (Johnston and Wessells, 1980; Solomon, 1981). such as NGF” (Varon and Bunge, 1978; Greene and The role of cell-substratum adhesion in the initiation, Shooter, 1980; Vinores and Guroff, 1980), contact guid- elongation, and branching of axons from either embry- ance (i.e., fasciculation) (Johnston and Wessells, 1980; onic or neonatal sympathetic, parasympathetic, or sen- Buskirk et al., 1980), and the physicochemical interaction sory neurons or from neuronal tumor cell lines has been of actively growing nerve fibers with the various sub- the object of numerous in vitro studies (Luduena, 1973; Helfand et al., 1976; Letourneau, 1975a, b, 1979; Schubert ’ This work was supported by United States Public Health Service and Whitlock, 1977; Schubert et al., 1978; Collins, 1978a, Research Grant EY-02186. We wish to thank I. S. Wood and M. T. b, 1980; Collins and Garrett, 1980; Hawrot, 1980; Adler Maglio for the transmission and scanning electron microscopy (facilities supported by Core Grant EY-02162). We would also like to thank Dr. and Varon, 1981). These studies have led to the conclu- B. Howard (UCLA) for initially describing the PC12 cells to us. The sion that there is a strong correlation between substra- invaluable assistance of H. Scodel in the preparation of the manuscript tum adhesion and enhanced neuronal morphogenesis. is gratefully acknowledged. This suggests that the adhesive interaction between the * To whom correspondence should be addressed at Cancer Research nerve cells and their microenvironment could be a crucial Institute, M 1282, University of California, Medical Center, San Fran- part of the initiation and elongation of neurons. Regula- cisco, CA 94143. tion of neuronal morphogenesis therefore may be ex- a The abbreviations used are: Ara C, cytosine arabinoside; BCE, pressed in part through the physicochemical properties bovine cornea1 endothelial; dbcAMP, dibutyryladenosine 3’:5’-cyclic of the interacting cell surface and its extracellular envi- monophosphate; DMEM, Dulbecco’s modified Eagle’s medium; DPBS, ronment. However, in most cases, the substrata consid- Dulbecco’s phosphate-buffered saline; DTT, dithiothreitol; ECM, ex- tracellular matrix; EDTA, ethylenediaminetetra-acetate; FGF, fibro- ered have been artificial in nature, consisting of plastic, blast growth factor; GuHCl, guanidine-HCl; HN02, nitrous acid, NGF, chemically modified surfaces (palladium-, polyorni- nerve growth factor; NHdOH, ammonium hydroxide; PBS, phosphate- thine-, or polylysine-coated surface), or collagen gels, as buffered saline; SDS, sodium dodecyl sulfate; TCA; trichloroacetic acid. well as killed non-neuronal cells and uncharacterized 1157 1158 Fujii et al. Vol. 2, No. 8, Aug. 1982 substratum-associated material produced by non-neu- twice) were from Sigma (St. Louis, MO). Chondroitinase ronal cells. ABC was obtained from Miles Laboratories (Elkhart, Cultured bovine cornea1 endothelial cells retain their IN). Collagenase was from Worthington Biochemical ability to produce an extensive ECM (Gospodarowicz Corp. (Freehold, NJ). Human plasma fibronectin was and Greenburg, 1981). This ECM, as characterized in from Collaborative Research (Waltham, MA) and bovine previous studies, is composed of collagen types 1:III:IV skin collagen (Vitrogen 100, 95% type I and 5% type III) and V present at a ratio of 3:16:1 (Tseng et al., 1981). was obtained from Collagen Corp. (Palo Alto, CA). Gel- Associated with the collagens are proteoglycans and gly- vatol 20-30 (polyvinyl alcohol) was obtained from Mon- cosaminoglycans that consist of heparan and chondroitin santo (St. Louis, MO). SDS and sucrose were from Bio- sulfates (Gospodarowicz and Greenburg, 1981; Nevo et Rad (Richmond, CA) and ultrapure urea was obtained al., 1982). Fibronectin and laminin (a marker for basal from Schwartz/Mann (Orangeburg, NY). Ampholine (pH lamina; Timpl et al., 1979) also are present (Gospodarow- 3.5 to 10) was purchased from LKB Instruments (Rock- icz et al., 1978, 1981). This ECM therefore has the bio- ville, MD), and Nonidet P-40 was purchased from Par- chemical composition of a basal lamina composed of a ticle Data, Inc. (Elmhurst, IL). [35S]Methionine (800 to lamina lucida and a lamina densa (Foidart et al., 1980; 1300 Ci/mmol) was from Amersham Corp. (Arlington Gospodarowicz et al., 1981). Heights, IL). The ability of cultured BCE cells to produce a matrix Cell culture conditions. The clonal rat pheochromo- similar to those found in viva gives us an opportunity to cytoma line, PC12, was the generous gift of Dr. Lloyd A. study the properties of a natural substratum with regard Greene (New York University Medical Center). Cultures to nerve cell adhesion and the subsequent neurite initi- were maintained as described by Greene and Tischler ation and outgrowth. It also allows us to study how the (1976) with the addition of Garamycin. Cells were grown response of nerve cells to trophic and chemotactic agents, in RPM1 1640 supplemented with 10% heat-inactivated such as NGF, may differ from the response previously horse serum, 5% fetal bovine serum, 2 mM glutamine, 50 observed when cells were maintained on various artificial pg/ml of Garamycin, 100 units/ml of penicillin, and 100 substrata. pg/ml of streptomycin (growth medium). Cultures were The rat pheochromocytoma cell line PC12, which maintained at 37” C in a humidified 5% CO2 incubator. shares many properties with cultured sympathetic gan- Stock cultures (30 ml) had one-half of the medium vol- glion cells (Greene and Shooter, 1980), was selected to ume changed three times weekly. Stock cultures with a study the role of cell-substratum interaction in regulating cell density of 2.5 to 3 x lo5 cells/ml were used to initiate nerve cell attachment, neurite outgrowth, and protein all experiments. Experimental cultures had one-half of synthesis. The advantage of using PC12 cells instead of the volume changed every other day with NGF added if normal sympathetic neuronal cells is that, although these previously present. cells do not require NGF in order to survive, they have The University of California, San Francisco Cell Cul- been shown to respond to it by initiating de nouo neurite ture Facility screened stock cultures for Mycoplasma by outgrowth on certain substrata (Greene and Tischler, DNA staining (Chen, 1977), culturing (McGarrity et al., 1976). 1979), and fluorescent antibody staining (Barile et al., 1973). The results were negative. The screening for other Materials and Methods microbial contaminations was also negative. Cultures of BCE cells were established from steer eyes Materials. DMEM (H-16), DPBS, glutamine, methi- as already described (Gospodarowicz et al., 1977; Gos- onine-free RPM1 1640, PBS, penicillin, RPM1 1640, and podarowicz and Greenburg, 1979). Stock cultures were streptomycin were obtained from Grand Island Biological maintained in the presence of DMEM supplemented Co. (Grand Island, NY). Horse serum (heat inactivated) with 10% fetal bovine serum and 5% calf serum, 2 mM was obtained from KC Biologicals, Inc. (Lenexa, KS). glutamine, 2.5 fig/ml of Fungizone, and 50 pg/ml of Calf serum and fetal bovine serum were from Irvine Garamycin in a humidified 10% CO, incubator. BCE Serum Co. (Irvine, CA). Tissue culture plastic dishes cultures used to coat plastic dishes with an ECM were (Falcon) were from Becton-Dickinson Labware, (Oxnard, grown as described above but with 10% calf serum and CA), Garamycin was from Schering-Plough Corp. (Ken- 5% dextran. Bovine vascular endothelial cell cultures ilworth, NJ), and Fungizone was from E. R. Squibb & were established from adult bovine aortic arch (Gospo- Sons, Inc. (Princeton, NJ). darowicz et al., 1976). Cell stocks were maintained rou- Mouse 7s and P-NGF were generously provided by tinely in DMEM supplemented with 10% calf serum, 2 Drs. L. F. Reichardt, K. Greif, and D. Shelton (University mM glutamine, 2.5 pg/ml of Fungizone, and 50 pg/ml of of California, San Francisco).
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